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Original article

The time course of in vivo recovery of transverse


strain in high-stress tendons following exercise
Scott C Wearing,1 James E Smeathers,2 Sue L Hooper,3 Simon Locke,3 Craig Purdam,4
Jill L Cook5
1
Faculty of Health Sciences ABSTRACT evaluated the effect of exercise training on the ‘elastic’
and Medicine, Bond University, Objective To evaluate the time course of the recovery properties of tendon (ie, stiffness and modulus), and
Gold Coast, Queensland,
Australia of transverse strain in the Achilles and patellar tendon have largely overlooked the ‘viscous’ component of
2
Institute of Health and following a bout of resistance exercise. tendon behaviour. Like many human tissues, tendons
Biomedical Innovation, Methods Seventeen healthy adults underwent are known to exhibit viscoelastic behaviour and sus-
Queensland University of sonographic examination of the right patellar (n=9) and tained static or cyclic loading has been shown to
Technology, Kelvin Grove,
Achilles (n=8) tendons immediately prior to and result in increasing strain or creep in tendon.18
Queensland, Australia
3
Centre of Excellence for following 90 repetitions of weight-bearing quadriceps With the advent of high-resolution ultrasound
Applied Sport Science and gastrocnemius-resistance exercise performed against systems, recent in vivo studies have noted an imme-
Research, Queensland an effective resistance of 175% and 250% body weight, diate decrease in the thickness of human tendon
Academy of Sport, Sunnybank, respectively. Sagittal tendon thickness was determined after bouts of cyclic resistance exercise and follow-
Queensland, Australia
4
Department of Physical 20 mm from the enthesis and transverse strain, as ing activities involving prolonged walking and
Therapies, Australian Institute defined by the stretch ratio, was repeatedly monitored running.19–24 Equating to transverse strains (TSs) of
of Sport, Canberra, Australian over a 24 h recovery period. around 10–20% in vivo, this acute change in thick-
Capital Territory, Australia
5
Results Resistance exercise resulted in an immediate ness has been hypothesised to reflect fluid move-
Faculty of Medicine, Nursing
decrease in Achilles (t7=10.6, p<0.01) and patellar ment associated with load-induced alignment of the
and Health Sciences, Monash
University, Frankston, Victoria, (t8=8.9, p<0.01) tendon thickness, resulting in an solid phase of the tendon matrix and is consistent
Australia. average transverse stretch ratio of 0.86±0.04 and 0.82 with creep behaviour reported with ex vivo testing
±0.05, which was not significantly different between of animal soft tissues, albeit in a transverse rather
Correspondence to tendons. The magnitude of the immediate transverse than in an axial direction.18 25–27 While the creep
Dr Scott C Wearing, Faculty of
Health Sciences and Medicine, strain response, however, was reduced with advancing response in soft tissues has been associated with
Bond University, Gold Coast, age (r=0.63, p<0.01). Recovery in transverse strain was reduced muscular activity and electromechanical
QLD 4229, Australia; prolonged compared with the duration of loading and delay and has been implicated in the development
swearing@bond.edu.au exponential in nature. The average primary recovery time of overuse injuries,14 surprisingly little is known
Accepted 3 February 2013
was not significantly different between the Achilles (6.5 about the time course of the creep recovery of soft
Published Online First ±3.2 h) and patellar (7.1±3.2 h) tendons. Body weight tissues following exercise. Of the few studies under-
23 March 2013 accounted for 62% and 64% of the variation in recovery taken to date, most have investigated the axial creep
time, respectively. recovery of the intervertebral disc in vitro and have
Conclusions Despite structural and biochemical observed that full recovery of the disc occurs only
differences between the Achilles and patellar tendon, the when the unloaded recovery time is one to several
mechanisms underlying transverse creep recovery in vivo orders of magnitude longer than loading.26 28 29
appear similar and are highly time dependent. These To the best of our knowledge, however, no study
novel findings have important implications concerning has evaluated the postexercise recovery of human
the time required for the mechanical recovery of high- tendon in vivo. Characterising postload recovery is
stress tendons following an acute bout of exercise. not only important for understanding the unloaded
tendon but is also critical to understanding tendon
behaviour under subsequent loadings. The aim of
INTRODUCTION this study, therefore, was to characterise and
Little is known about the adaptive response of compare the time course of the postexercise recov-
human patellar tendon to loading. Originally con- ery in TS in the Achilles and patellar tendon in
sidered metabolically inert, recent studies have vivo. These tendons are thought to function as
shown acute loading of human tendon results in elastic-energy-storage springs during locomotion
increased intratendinous glucose uptake, oxygen and in addition to experiencing relatively high
consumption, blood flow and collagen turnover in stress levels during activities of daily living are
peritendinous tissues and the expression of certain prone to chronic ‘overuse’ injury and degenerative
genes, growth factors and mediators of inflamma- change.30 31 We hypothesised that, as with other
tion.1–6 However, the effect of loading on the human soft tissues, full recovery of the Achilles and
mechanical properties of tendon is less clear. While patellar tendons would occur within 24 h following
most studies have observed that habitually active exercise and that recovery times would not differ
individuals possess larger tendons (20–36%) than between tendons.
their untrained counterparts,7–9 prospective studies
To cite: Wearing SC, have shown that exercise training either METHODS
Smeathers JE, Hooper SL, increases,10–12 decreases13 14 or has no effect on Subjects
et al. Br J Sports Med measures of tendon stiffness and modulus in Seventeen healthy adults were recruited from uni-
2014;48:383–387. vivo.15–17 These studies have, however, typically versity faculty to participate in this repeated

Wearing SC, et al. Br J Sports Med 2014;48:383–387. doi:10.1136/bjsports-2012-091707 1 of 6


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Original article

measures study, which received approval from the institutional


review board. Study exclusion criteria included a medical
history of diabetes, inflammatory joint disease, familial hyper-
cholesterolaemia or lower limb tendon pathology. No partici-
pants were excluded. All participants were non-medicated,
non-smokers and recreationally active based on self-report and
presented to the laboratory having abstained from physical activ-
ity in the previous 24 h. Participant numbers were based on pre-
viously published data for human Achilles tendon19 and were
sufficient to detect a 10% difference in the immediate TS
response of the two tendons (α=0.05, β=0.20). Body height
was measured to the nearest millimetre using a stadiometer and
weight was recorded to the nearest gram using clinical scales.
Body mass index (BMI) was calculated by dividing body
weight (kg) by the square of body height (m).

Sonographic imaging
Sonographic examination of the Achilles and patellar tendons
was undertaken by an experienced operator using a 10 MHz
linear array transducer (Echoblaster 128, UAB Telemed, Vilnius,
Lithuania) and standardised protocol. The accuracy and preci-
sion of the ultrasound system was evaluated by undertaking
repeated measurements of a standard calibration phantom
(040GSE, CIRS, Norfolk, Virginia, USA), consisting of a
number of Nylon monofilaments of varying diameters Figure 1 Tendon thickness was measured from sagittal sonograms at
(0.1–8 mm) and depths embedded within a tissue-mimicking standard reference sites and with the aid of a greyscale profile. Achilles
material (attenuation: 0.5±0.05 dB/cm-MHz). The 95% limits tendon thickness was determined 20 mm superior to its calcaneal
of agreement for repeated measures of 27 separate calibration (C) insertion (a). Patellar tendon thickness was measured 20 mm distal
monofilaments were ±100 mm, with a root mean square (RMS) to the inferior pole (P) of the patella (b).
error of 184 mm.
In accordance with recommendations, longitudinal sonograms
of each tendon were acquired perpendicular to the point of thickness was determined at a standard site, 20 mm distal to its
maximum tendon width to encompass the superior aspect of attachment at the inferior pole of the patellar,32 while Achilles
the calcaneus and distal Achilles tendon and the inferior aspect tendon thickness was determined 20 mm proximal to its calca-
of the patella and proximal patellar tendon (figure 1).32 Sagittal neal insertion. The anterior and posterior edges of the tendons
images of the Achilles tendon were acquired with the participant were identified with the aid of a grey-scale profile, and manually
prone and the ankle passively positioned at 90°,33 while sagittal digitised (figure 1). The stretch ratio (λ), the ratio of postexercise
plane images of the patellar tendon were acquired with the par- to pre-exercise tendon thickness, was subsequently calculated as
ticipants supine with their leg passively positioned at right a measure of TS. The stretch ratio is commonly used in the ana-
angles (90°) to their thigh.32 Sonographic images were taken lysis of materials that exhibit large deformations and approxi-
immediately prior to and following completion of 90 repetitions mates to engineering strain (ɛ) by; ɛ=1−λ. The coefficient of
of resistance exercise and repeated during recovery at 3, 6, 12 variation for repeated measures of tendon thickness was 2.3%
and 24 h postexercise for the Achilles tendon and at 3, 6 and and 2.6% for the Achilles and patellar tendons, respectively.
24 h postexercise for the patellar tendon. Although biexponential models have been used to describe
the two phase recovery behaviour of collagenous tissues such as
intervertebral disc,26 28 a single-term exponential recovery func-
Exercise protocol tion can also be used to successfully model creep recovery in
Following pre-exercise sonograms, participants randomly com- other human soft tissues.37 Hence, the recovery in TS following
pleted closed kinetic chain resistance exercises involving the exercise was modelled for each participant using a single-term
Quadriceps (n=9) or Gastrocnemius (n=8) muscle groups. exponential function; TS(t) = λo + λe(−βt), where constants λo,
Quadriceps exercises consisted of 90 repetitions of double-leg λ and β represent the initial stretch ratio, the range and the rate
squat exercises in which participants moved from standing erect, to of recovery, respectively, and were estimated using non-linear
a position of 90° of knee flexion and then back again.34 Ankle exer- regression and minimising RMS error. The time for the tendon
cises consisted of 90 repetitions of double-leg calf raises in which to return to 63% of pre-exercise dimensions, the so-called
participants moved their foot from full ankle plantarflexion to full primary recovery time, was estimated as the inverse of the
dorsiflexion and then back again with their knee in an extended β term for each participant.
position.35 Quadriceps exercises were performed against an effect- The Statistical Package for the Social Sciences (SPSS Inc,
ive resistance of 175% body weight and ankle exercises against an Chicago, Illinois, USA) was used for all statistical procedures. As
effective resistance of 250% body weight, so as to induce tensile outcome variables were determined to be normally distributed,
loads similar to that experienced during gait.34–36 means and SDs have been used as summary statistics.
Between-group differences in body anthropometry were investi-
Data reduction and statistical analysis gated using independent t tests. Differences in tendon thickness
Sonographic images were analysed using MATLAB software immediately pre-exercise and postexercise were investigated
(MathWorks Inc, Natick, Massachusetts, USA). Patellar tendon using paired t tests. Differences in the TS response and recovery

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Original article

Table 1 Demographic characteristics of participants completing


Achilles and patellar tendon exercises
Achilles tendon Patellar tendon

N 8 9
Age (years) 39.7 (9.3) 33.3 (11.1)
Height (cm) 176.9 (3.3) 174.9 (7.6)
Weight (kg) 76.8 (8.4) 75.6 (13.8)
BMI (kg/m2) 24.5 (2.1) 24.6 (3.6)
BMI, body mass index.

time between the Achilles and patellar tendons were investigated


using independent t tests. Relationships between variables were
investigated using Pearson product–moment correlations. An α Figure 3 Recovery curves for the acute transverse strain of the
level of 0.01 was used. Achilles (▪) and patellar (°) tendons following resistance exercise.

RESULTS
Anthropometric characteristics of participants are summarised The average primary recovery time was 6.5±3.2 h for the
in table 1. There was no statistically significant difference in Achilles tendon and 7.1±3.2 h for the patellar tendon and was
average age, height or weight of participants performing the not significantly different between tendons. Recovery was,
two exercise protocols. however, dependent on body weight (p<0.01), with greater
The average thickness of the Achilles and patellar tendons body weight associated with prolonged primary recovery in TS
prior to exercise was 4.0±0.4 and 3.2±1.2 mm, respectively. (figure 4). This relationship was also exponential in nature, with
While the Achilles tendon was, on average, 27% thicker than body weight accounting for 62% and 64% of the variation in
the patellar tendon at baseline, this difference was not statistic- primary recovery time of the patellar and Achilles tendons,
ally significant. respectively.
Resistance exercise resulted in a significant and immediate
decrease in the sagittal thickness of the Achilles (t7=10.6, DISCUSSION
p<0.001) and patellar (t8=8.9, p<0.001) tendons of all partici- The Achilles and patellar tendons are widely regarded to func-
pants, resulting in an average stretch ratio of 0.86±0.04 and tion as springs, storing and elastically returning strain energy
0.82±0.05, respectively. This difference in TS response between during locomotion, which is thought to improve the efficiency
the two tendons was not statistically significant. Similarly, of gait and protect against muscle damage during rapid and
there was no significant correlation between anthropometric forceful lengthening. Although these tendons are exposed to
measures (height, weight and BMI) and transverse stretch ratio high levels of stress during life and are prone to chronic
(r=0.22–0.39). However, participant age was moderately corre- ‘overuse’ injury,31 little is known regarding their acute response
lated with the magnitude of the immediate TS response in the to exercise or the time course of their recovery postexercise.
Achilles and patellar tendons (r=0.63, p<0.01), such that older The findings of the current study indicate that resistance exer-
age was characterised by a diminished TS response (figure 2). cise results in an immediate but transient decrease (14–18%) in
Although tendon dimensions returned to pre-exercise levels the thickness of the Achilles and patellar tendons, that is, recov-
for both tendons within 24 h, recovery in TS was exponential in erable within 24 h.
nature (figure 3). The R2 goodness-of-fit for the overall model Acute reductions in tendon thickness have been previously,
was 0.99 for both the Achilles and patellar tendons, with the R2 though not exclusively,38 39 observed following intense or pro-
fit for individual TS–recovery curves exceeding 0.93 in all cases. longed exercise in vivo.19–24 Hypothesised to largely reflect the

Figure 4 Relationship between body weight and the primary recovery


Figure 2 Effect of age on the immediate transverse strain of the time of the Achilles (▪) and patellar (°) tendons following resistance
Achilles (▪) and patellar (°) tendons in response to exercise. exercise.

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Original article

movement of fluid associated with load-induced alignment of Gedalia et al64 observed that feline lumbar structures recovered
the solid phase of the tendon matrix, the findings of the current by only 37% with rest lasting more than twice the duration of
study are consistent with in vitro observations in animal models creep loading (2 h). Similarly, Solomonow et al26 observed that
in which static and cyclic loading have been shown to result in 50 min of cyclic load induced axial creep in the feline lumbar
reduced tendon thickness, rapid unbinding and extrusion of spine that required more than 7 h to recover (>90%).
intratendinous fluid and visible loss of water and glycosamino- The primary recovery time of the Achilles and patellar
glycans.40–42 These observations are also consistent with axial tendons in the current study was, in part, dependent on the par-
creep behaviour, manifest as an increase in axial length ticipant’s body weight. Greater mass was associated with a pro-
with cyclic load, reported with mechanical testing of both longed primary recovery in transverse tendon strain (figure 4).
animal18 25–27 and human soft tissues in vitro,27 28 and follow- Although delayed physiological recovery in markers of skeletal
ing loading of human tendon, ligament and intervertebral disc muscle metabolism and perfusion have been observed following
in vivo.43–45 exercise in the obese,65 in vitro studies on the mechanical
Axial creep in tendon has been suggested to alter the poten- behaviour of the human vertebral disc have also demonstrated
tial of muscle to generate force, via both direct mechanical that the creep recovery is influenced by the magnitude and dur-
and neuromuscular effects, and thereby increase the risk of ation of the applied load.28 In the current study, exercises were
injury.46 47 Although the mechanisms underpinning the creep performed against a percentage of body weight. Consequently,
response of soft tissues are poorly understood, Vresilovic et al48 it is unknown if the relationship between body weight and the
proposed that, for the intervertebral disc, the magnitude of recovery of transverse strain in the Achilles and patellar tendons
dynamic creep was dependent on the quantity of fluid within reflects physiological processes associated with greater mass or
the fluid-flow pathway, and demonstrated marked changes in merely greater mechanical loading of the tendon during exer-
creep of the disc with manipulation of tissue hydration. While cise. Further research, specifically evaluating the creep recovery
comparable effects of hydration have been observed on the of tendon to a varied strain stimulus seems warranted.
relaxation behaviour of tendon in vitro,49 in the current study The present experimental setup did not allow for a mechanistic
exercise induced a similar magnitude of TS in both the Achilles explanation for the observed recovery in TS following exercise.
(1−λ, 0.14) and patellar (1−λ, 0.18) tendons, suggesting that the However, previous in vivo studies in humans have shown that a
pathway and unbound fluid content of the two tendons are likely single bout of loading initiates a cascade of physiological events
comparable. In support, Maynard et al50 demonstrated that the postexercise, including increased intratendinous blood volume
water content of the rabbit Achilles tendon (59% wet weight) and glucose uptake and the expression of certain genes, growth
did not differ from that of the patellar tendon (63% wet factors and mediators of inflammation.1 5 6 66 Although markers
weight), despite obvious differences in the ultrastructure of the two of collagen metabolism peak after the primary recovery times
tendons and subtle differences in cellular properties and respon- noted in this study,67 the time course of postexercise circulatory
siveness, collagen crimp, interstitial space and glycosaminoglycan and inflammatory responses appear similar to the recovery in
concentration.51–54 transverse tendon strain. For instance, intratendinous blood
A novel finding of the current study was that the magnitude volume in the Achilles tendon has been shown to increase imme-
of the TS response of the two tendons following exercise was diately following a series of isometric muscle contractions and
moderately correlated with age. Older age was associated with a remain elevated for at least 20 min after exercise.66 Similarly,
reduced TS response. Based on the regression equation, each cyclic loading of ligament and tendon in animal models has been
decade of life was associated with a ≈2.5% reduction in the TS shown to increase the mRNA expression of inflammatory media-
response of the Achilles and patellar tendons. Changes in tors immediately postexercise,68 which return to basal levels in
the composition of tendon, including increased collagen cross paratendonous tissues within 6–12 h of exercise.69 70 It is pos-
linking, altered fibril morphology, decreased glycosaminoglycan sible, therefore, that a reactive hyperaemia and/or inflammatory
concentration and lower water content are known to occur with processes may collectively or individually drive imbibition of
aging.55–58 Given that load-induced fluid movement has been fluid in tendon and thereby the recovery of tendon dimensions.
hypothesised to play a key role in tendon homeostasis and that As such, tendon recovery may reflect active rather than passive
tendinopathy is characterised by a reduced TS response to exer- processes. However, the time constants for the overall recovery
cise,59 60 it is possible that diminished load-induced fluid move- of the patellar and Achilles tendons in the current study (≈6–7 h)
ment with aging, as evidenced by a lower TS response to are comparable to those reported for recovery of axial strain of
exercise, may in part account for the impaired ability of tendon the intervertebral disc when studied in vitro (≈8 h),28 suggesting
in the elderly to adapt to training and the greater incidence of that recovery in transverse tendon strain in vivo may be governed
tendon degeneration and rupture with advancing age.61 62 by passive osmotic and ionic forces.
However, age accounted for only 40% of the variation in the This study evaluated the recovery of transverse tendon strain
TS response of tendon to exercise, suggesting that other, as yet following resistance exercise protocols that involved periodic
unidentified, factors also influence the transverse creep response concentric and eccentric modes of muscle contraction. While
of tendon to exercise. there is some evidence that aerobic exercise may elicit greater
Recovery of TS, as defined by the stretch ratio, in the Achilles tendon hypertrophy than resistance exercise over a 12-week
and patellar tendons in the current study followed an exponen- period,62 the time course of tendon recovery observed in the
tial pattern and was several orders of magnitude longer (hours) current study may not be transferable to other types and modes
than the duration of the exercise (minutes). The average time of exercise. There is evidence, for instance, that both the mode
for primary recovery of the Achilles and patellar tendons follow- (eccentric/concentric) and duration of muscle contraction may
ing exercise was 6.5±3.2 h and 7.1±3.2 h, respectively. This influence blood flow and the magnitude of creep in tendon.19 66
finding is consistent with in vitro studies on the axial creep of Nonetheless, the findings of the current study demonstrate that
skin and disc tissues,28 63 and similarly slow recovery rates, short periods of resistance exercise, involving cyclic concentric
albeit in axial strain, have been reported in vivo for other bio- and eccentric contraction, induce substantial TSs in healthy
logical tissues following mechanical loading in animal models. human Achilles and patellar tendons. While the time course of

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Original article

the recovery of tendon dimensions is considerably longer than manuscript. SLH contributed to the study design, analysis and interpretation of data,
the loading duration, with a primary recovery time of around revision and the final approval of the manuscript. SL contributed to the study
design, analysis and interpretation of data, revision and the final approval of the
7 h, the optimal schedule of activity and rest ratios in these manuscript. CP contributed to study conception and design, analysis and
high-stress elastic-storage tendons is still unknown, and requires interpretation of data, revision and the final approval of the manuscript. JLC
attention in light of the knowledge gained through this study. contributed to the study conception and design, analysis and interpretation of data,
revision and the final approval of the manuscript.
Funding This research was funded by an Australian Research Council Linkage Grant
CONCLUSION (LP_0989716).
In vivo recovery of TS in the Achilles and patellar tendons fol-
Competing interests SCW is funded through a Smart Futures Fellowship,
lowing resistance exercise of the quadriceps and gastrocnemius Department of Employment, Economic Development and Innovation, Queensland
muscle groups is considerably longer than the loading duration, Government.
with primary recovery in both tendons requiring around 7 h. Patient consent Obtained.
These findings suggest that, despite their structural differences,
Ethics approval The study was approved by the regional ethics committee. QUT
the mechanisms underlying Achilles and patellar tendon UHREC (Approval Number: 1000000857).
mechanics in vivo are similar and highly time-dependent.
Provenance and peer review Not commissioned; externally peer reviewed.
Although further work is required, these findings highlight, for
the first time, the duration of recovery required for high-stress
tendons to return to pre-exercise dimensions following an acute
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6 of 6 Wearing SC, et al. Br J Sports Med 2014;48:383–387. doi:10.1136/bjsports-2012-091707


Downloaded from http://bjsm.bmj.com/ on January 25, 2015 - Published by group.bmj.com

The time course of in vivo recovery of


transverse strain in high-stress tendons
following exercise
Scott C Wearing, James E Smeathers, Sue L Hooper, Simon Locke,
Craig Purdam and Jill L Cook

Br J Sports Med 2014 48: 383-387 originally published online March 23,
2013
doi: 10.1136/bjsports-2012-091707

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