597

ORIGINAL ARTICLE

Br J Sports Med: first published as 10.1136/bjsm.2003.007120 on 23 September 2004. Downloaded from http://bjsm.bmj.com/ on July 6, 2022 by guest. Protected by copyright.
Running exercises improve the strength of a partially
ruptured Achilles tendon
E K N See, G Y F Ng, C O Y Ng, D T C Fung
...............................................................................................................................
Br J Sports Med 2004;38:597–600. doi: 10.1136/bjsm.2003.007120

Objectives: To examine the effects of running and swimming exercises on the functional performance and
mechanical strength of a recovering Achilles tendon.
Methods: 30 Sprague-Dawley rats had surgical transection of their right medial Achilles tendon. The rats
were divided into running (n = 11), swimming (n = 10), and control (n = 9) groups. The running and
See end of article for swimming groups were given daily exercise training, starting from the fifth day after the injury; the control
authors’ affiliations group did not exercise throughout the period of the experiment. An Achilles functional index (AFI) was
....................... recorded before the operation and on the third, 10th, and 30th days after the operation. On the 30th day,
Correspondence to: the rats were killed and their Achilles tendons harvested for biomechanical testing of load relaxation
Professor Gabriel Ng, properties, stiffness, and ultimate tensile strength (UTS). The AFI data were analysed by two way analysis
Department of of variance; load relaxation, stiffness, and UTS data were analysed by multivariate analysis, with a at
Rehabilitation Sciences, 0.05.
The Hong Kong
Polytechnic University, Results: The UTS of the running group was higher than in the control group (p = 0.015), while there was no
Hung Hom, Kowloon, significant difference between the swimming and control groups (p = 0.228). Differences in stiffness and
Hong Kong; load relaxation were non-significant (p = 0.823 and 0.633, respectively). The AFI results did not differ
rsgng@polyu.edu.hk
among the three groups (p = 0.242).
Accepted 27 June 2003 Conclusions: Running exercises can improve the strength of partially ruptured Achilles tendons at 30 days
....................... after injury.

T
endons heal slowly after injury, and the rupture of ligament were significant with enforced exercises,10 11 but the
Achilles tendons usually means weeks of immobilisation same effect was not demonstrated in tendons during healing.
with or without surgical repair.1 However, immobilisa- Murrel et al reported that 15 minutes of daily swimming
tion of the ankle joint, even for a short time, has an adverse exercise had no effect on the biomechanical properties of
effect on function, biochemical properties, and biomechanical healing tendons as compared with a non-exercised group.12
strength of both normal and injured Achilles tendons in the However, the non-significant results of Murrel’s study did
rat.2 3 Early functional loading and controlled movements not necessarily infer that exercise training was unable to
have been reported to augment the strength of healing improve tendon strength. The negative results could have
Achilles tendons without causing them to re-rupture.4–6 reflected other factors such as the mode of injury, as the
Enwemeka et al reported that rats starting weight bearing researchers had used a complete sectioning injury model of
exercises five days after Achilles tendon injuries had a all plantar flexors. This had caused the cut ends of the
significantly higher breaking strength in the tendons than tendons to retract, thus rendering healing difficult.
control animals or rats that began exercising two days after Furthermore, the duration of the exercise or the type of
the injury.6 The same investigators5 also reported that loading might not have been large enough to lead to any
functional loading beginning five days after tenotomy led effects. The exercises could have begun too early, as the
to a significant increase in the tensile strength and energy animals were put to swim immediately after the injury when
absorption capacity of the Achilles tendons of rabbits. Date4 inflammation was still intense, which might have caused the
studied the effect of loading on the ultrastructure of healing inflammation to flare up, leading to overscarring and
tendons and showed that the diameter of the collagen fibres abnormal tissue strength.
increased, suggesting a more rapid collagen maturation In view of the above, it is necessary to conduct a study to
process. simulate the conditions of partial tendon rupture, so that the
It has been found that in normal tendons the concentra- cut ends are not retracted and healing is not impeded.13 The
tion of collagen, the size of collagen fibrils, and fibril density exercises should also be delayed for a few days to avoid
increase after exercise.7 These ultrastructural morphological
aggravating the acute inflammation.14 To date, no study has
changes are manifested by mechanical improvement in the
been reported comparing the effects of different types of
tendons, and it has been well documented that the ultimate
exercise on a partially injured tendon. Furthermore, the
tensile strength of normal tendons increases with swimming
viscoelastic properties of repairing tendons have not been
and running.8 9 Simonsen et al showed that the ultimate
investigated; thus their behaviour under sustained loading is
tensile strength of tendons in swimming trained animals was
not known. We therefore conducted this study to examine
significantly higher than in their strength trained counter-
the effects of exercise on the biomechanical and functional
parts.9 Tendons seem to respond to endurance exercises but
properties of the partially injured Achilles tendons of rats,
not to high loading strength training. These effects of exercise
training might also be manifested in tendons under repair.
However, only a few studies have examined the effects of
exercise on healing ligaments and tendons. Studies have ................................................................
shown that the effects of training on the tensile strength Abbreviations: AFI, Achilles functional index; UTS, ultimate tensile
and biochemical properties of transected medial collateral strength

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598 See, Ng, Ng, et al

and to compare the effects of weight bearing and non- a walkway 10 cm wide and 60 cm long with a white paper

Br J Sports Med: first published as 10.1136/bjsm.2003.007120 on 23 September 2004. Downloaded from http://bjsm.bmj.com/ on July 6, 2022 by guest. Protected by copyright.
weight-bearing exercises on tendons that are healing. underlay. Their hind paws were dipped in blue paint, and the
rat was made to walk down the walkway, leaving blue
METHODS footprints on the white underlay surface. The papers were
Subjects coded by the animal’s number and stored to be measured
Thirty Sprague-Dawley rats aged three months were used. later in a single blind fashion.
Their average weight at the time of surgery was 472 g (range Measurements were taken from the middle four footprints
375 to 575). The animal subjects ethics review committee of marked on the paper. The maximum length of a foot print is
the Hong Kong Polytechnic University reviewed and defined as the print length factor (PLF), the distance between
approved the procedures of this study. the first and fifth toes is the toe spreading factor (TSF), and
Each rat had complete transection of the medial part of the the distance between the second and fourth toes is the
right Achilles tendon, leaving the lateral tendon intact as an intermediary test factor (ITF). These factors were measured
internal splint to prevent the cut ends from retracting. They and the AFI was calculated according to an established
were randomly divided into three groups: group 1, no formula15:
exercise (control); group 2, running exercises; group 3,
swimming exercises. AFI = 74(PLF) + 161(TSF) + 48(ITF) 2 5.

Surgical procedures Biomechanical testing

All surgical procedures were carried out under general The rats were killed on the 30th day after the operation by an
anaesthesia with an intraperitoneal injection of a mixture overdose injection of anaesthesia. Both lower limbs were
of 100 mg/kg ketamine and 20 mg/kg xylazine (both from harvested by disarticulating them at the hip joints. The
Alfasan International, Woerden, Netherlands). The dosages specimens were then sealed in a plastic bag and stored at
were calculated according to the ratio of 0.6 mg ketamine and –40˚C for later testing.
0.3 mg xylazine per 100 g body weight. The skin on the At least six hours before testing, the specimens were
anterior aspect of the right calf was shaved, incised, and retrieved from the freezer and allowed to thaw inside the
retracted to expose the Achilles tendon. The tendon of the plastic bag at room temperature. The specimens were
medial gastrocnemius was identified and separated from the dissected to remove all soft tissues, leaving the intramuscular
lateral tendon with a probe; the medial tendon was then tendinous fibres, Achilles tendon, and calcaneus intact. The
transected with a scalpel at its mid point. The lateral tendon intramuscular tendinous fibres were then secured between
and plantaris were left intact to simulate the case of a partial two strips of plastic with quick setting superglue. Care was
tendon rupture, so as to prevent the ruptured ends from taken to prevent the glue from running down the tendon,
retracting.13 The skin wound on the anterior calf was closed and the specimens were kept moist with normal saline
by a suture. After the operation, the animals were divided during the whole testing procedure.
into groups of five, each group being placed in a 20624640 The glued strip and the calcaneus were then mounted on
cm cage. No cast immobilisation was applied, and the rats the cross heads of a material testing machine (MTS Synergie
were allowed to move unhindered inside the cages. All the 200, MTS Systems, Minnesota, Minneapolis, USA). An
animals were kept under a 12 hour light/dark cycle, with extensometer (MTS model 634: 12F-24, MTS Systems) was
temperatures regulated at about 20˚C and relative humidity attached to the margin of the cross heads for measuring the
at 50%. Tap water and food were given ad libitum during the local strain in the tendon. The room temperature was
whole study. controlled at 25˚C throughout testing.

Exercise programme Testing for viscoelasticity

The timing of exercise followed a previous report.5 On the Each specimen mounted on the material testing machine was
fifth day after the operation, the two exercise groups began preconditioned with 10 oscillation cycles of 2.5% strain at a
their respective exercise programmes. All the rats in the rate of 10 mm/min to eliminate the effect of deep freezing on
running group ran on a treadmill at an initial speed of the tissue.17 18 After preconditioning, the specimen was
4.0 m/min for the first two days of the exercise. This speed elongated to 2.5% strain and maintained for five minutes.19
was used in order to acquaint the rats with the running The loads were recorded throughout the test at a sampling
exercise. The speed was gradually increased to 12 m/min rate of 5 Hz. To quantify the load relaxation property, the
throughout the training period. The rats in the swimming difference between the initial and final load was expressed as
group swam in a rectangular water tank measuring a percentage of the initial load.
39670640 cm filled with water at 25˚C. The water level
was adjusted so that the rats could not touch the floor of the Testing for ultimate tensile strength
tank with their legs. After testing for viscoelasticity, the specimen was unloaded
All the animals in both exercise groups were exercised for and left for five minutes on the machine to let the tendon
six days a week, starting from the fifth day after the return to its original length. It was then subjected to the
operation until the 30th. The duration of the exercises was failure test at a loading rate of 500 mm/min until failure.19
progressively increased from 15 minutes in the first week to Load and displacement data were recorded at a sampling rate
17 minutes in the second week, and then to 19 minutes for of 50 Hz. The maximum load recorded represents the
the remainder of the time. ultimate tensile strength (UTS), and the gradient in the
linear portion immediately after the toe region of the load
Measurements displacement curve represents the stiffness value.
Functional testing
Functional testing of the Achilles tendon was done in all Statistical analysis
animals preoperatively and then on postoperative days 3, 10, The within-subject reliability of the AFI measurements was
and 30. We used the Achilles functional index (AFI), reported established with intraclass correlation coefficients,1 3 with
in the study by Murrel et al.15 This test has proved reliable and two measurements of the preoperative recording. A two way
sensitive to healing time, and shows excellent correlation repeated measures analysis of variance (ANOVA) was used to
with the properties of load to failure.16 The rats were tested in analyse the AFI data. A multivariate analysis of variance

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Running and tendon repair 599

(MANOVA) was used to analyse the load relaxation, UTS,

Br J Sports Med: first published as 10.1136/bjsm.2003.007120 on 23 September 2004. Downloaded from http://bjsm.bmj.com/ on July 6, 2022 by guest. Protected by copyright.
Table 1 Ultimate tensile strength (UTS), stiffness, and per
and stiffness data. The independent variable was the group- cent load relaxation in the three groups
ing. The significance level was set at 0.05 for all the tests.
Control Running Swimming
RESULTS (n = 9) (n = 11) (n = 10) p Value
On visual examination, the Achilles tendon in all groups UTS (N) 61.7
(12.6) 73.8
(9.0) 67.6 (9.7) 0.049*
showed signs of repair, with thick fibrous scar formation Stiffness (N/mm) 71.5 (18.0) 76.5 (15.9) 72.2 (24.3) 0.823
around the injury sites. The mean ICC for the preoperative Load relaxation (%) 38.4 (12.6) 37.7 (9.0) 40.5 (9.7) 0.633
AFI measurements was 0.97, which indicates good reliability
Values are mean (SD). The p values are derived from analysis of variance
for the AFI measurements. However, the result of the AFI (ANOVA).
was not significant among the three groups (p = 0.242). The *Significant difference in the ANOVA result.
AFI values of all groups fell from the values recorded on the
Significant difference with post-hoc linear contrasts for between-group
preoperative day to reach a low on postoperative day 3, and comparisons.
before gradually improving on days 10 and 30 (fig 1).
The results of load relaxation and stiffness were not and locomotion may augment the tensile strength of the
significantly different among the groups (p = 0.633 and Achilles tendon.5 6 The greater strength in tendons that had
p = 0.823, respectively). However, the difference in the UTS been subjected to exercise could reflect accelerated fibroblast
was significant (p = 0.049). Post hoc analysis showed that proliferation, fibrillogenesis, and matrix remodelling, because
the UTS of the running group was greater than in the control it is the collagen content and arrangement of the fibrils that
group (p = 0.015), while the value in the swimming group determines strength.23 24
did not differ from that in the control group (p = 0.228) Our finding that the load relaxation and stiffness of the
(table 1). running group did not differ from the control group could
have resulted from the low statistical power (,0.2) of our
DISCUSSION comparisons for both these variables. Furthermore, load
In this study we found that running exercises can promote relaxation is a viscoelastic property, whereas stiffness and
the recovery of partially transected Achilles tendon in rats. UTS are structural properties. It has been suggested that
Previous studies have shown that in the Achilles tendon of viscoelasticity is determined by the interaction between small
healing rabbits, inflammation subsides within seven days sized collagen fibrils, and structural properties by large sized
after injury, and fibroplasia and fibrillogenesis begin at about collagen fibrils.25 The non-significant difference in load
five days after the injury, with fibroblasts and newly relaxation among the three groups could indicate that
synthesised collagen scattering in the tissue.14 20 From 12 exercise has no effect on the ultrastructural morphological
days onward, collagen synthesis occurs concurrently with profile of the small collagen fibrils. This will need to be
matrix remodelling, characterised by the aggregation of the explored further with ultrastructural morphological studies.
collagen fibrils into bundles that are easily observable by day As for stiffness and UTS, the former is a measurement at
21.14 20 submaximal loading while the latter is a measurement of the
The high UTS of our running group could reflect maximum strength. Thirty days after injury, the tendons
accelerated fibroblast proliferation, fibrillogenesis, and might have recovered to such an extent that the submaximal
matrix remodelling as a result of the exercise loading on property was normal, so that no difference was found in
the tendon. In previous studies it has been shown that stiffness measurements.
mechanical loading can enhance the parallel alignment and As both stiffness and UTS are derived from the same load
polymerisation of the collagen fibrils and the production of deformation curve, differences in UTS but not in stiffness
glycosaminoglycans.21–23 Becker and Diegelmann21 reported among groups would imply a larger area under the curve, and
that the fibroblasts of tendons under loading were better thus a higher energy absorption capacity in the running
aligned than those of tendons without loading. On another group. This may be explained by the structural morphology.
study it was found that mechanical loading facilitated the Textural birefringence measurements in the tendons of
formation of intracytoplasmic collagen fibrils, a phenomenon exercised animals have shown that the process of adaptation
associated with the rapid synthesis of collagen, and that this to a new level of functional stimulation results in the
phenomenon was not shown in tendons immobilised by reorganisation of the extracellular matrix elements. At the
casts.22 Furthermore, the mechanical forces of weight bearing macromolecular level, this corresponds to better alignments
of the collagen bundles with more organised intermolecular
packing orders than those of the controls.23 Becker and
Diegelmann21 showed that fibroblasts were stretched out
parallel to the direction of tension compared with the random
orientation of control tendons without tension. Exercise
might have induced the fibres to reorientate to the extent
that they became able to withstand higher tensile forces and
absorb more energy before breakage.
The results of our swimming group are in line with the
findings of Murrel et al,12 who also reported no significant
benefits of swimming exercises for the strength of repairing
tendons. This could reflect the mechanical demands of the
swimming group. Although swimming is an active exercise,
the loading in the Achilles tendon is small because of its
non-weight-bearing nature. The small loading may not have
been enough to stimulate fibroblast proliferation and
Figure 1 The pattern of change in Achilles functional index (AFI) of the
fibrillogenesis.
control, running, and swimming groups on the preoperative day (Pre), Comparing our study with that of Burroughs and
postoperative day 3 (Post D3), day 10 (Post D10), and day 30 (Post Dahners,10 the exercise intensity for the swimming group
D30). was similar between the two studies, but the findings were

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600 See, Ng, Ng, et al

in close approximation, either in cases of partial rupture or

Br J Sports Med: first published as 10.1136/bjsm.2003.007120 on 23 September 2004. Downloaded from http://bjsm.bmj.com/ on July 6, 2022 by guest. Protected by copyright.
Take home message after surgical repair for total rupture.

N Exercise has been reported to improve the strength of ACKNOWLEDGEMENTS

We thank Dr Mason Leung for his technical advice and the
repairing tendons. However, it is not known whether
Department of Rehabilitation Sciences of The Hong Kong
exercise may benefit tendons with partial injury, and if Polytechnic University for its financial support of the study.
it does, what type of loading is of greatest benefit. This
study shows that running exercise can significantly .....................
strengthen a partially injured Achilles tendon, but this Authors’ affiliations
effect was not found with swimming exercise. E K N See, G Y F Ng, C O Y Ng, D T C Fung, Department of
Rehabilitation Sciences, The Hong Kong Polytechnic University,
Kowloon, Hong Kong

different. Burroughs and Dahners found that enforced

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