Published Online January 25, 2012
Immediate and short-term effects of exercise
on tendon structure: biochemical,
biomechanical and imaging responses
Alex Tardioli, Peter Malliaras, and Nicola Maffulli *
Centre for Sports and Exercise Medicine, Barts and the London School of Medicine and Dentistry,
Mile End Hospital, 275 Bancroft Road, London E1 4DG, UK
Introduction: Tendons are metabolically active structures, and their biochemical,
biomechanical and structural properties adapt to chronic exercise. However,
abnormal adaptations may lead to the development of tendinopathy and pain.
Acute and subacute adaptations might contribute to tendon pathology.
Sources of data: A systematic search of peer-reviewed articles was performed using
a wide range of electronic databases. A total of 61 publications were selected.
Areas of agreement: Exercise induces acute responses in collagen turnover, blood
flow, glucose, lactate and other inflammatory products (e.g. prostaglandins and
interleukins). Mechanical properties are influenced by activity duration and
intensity. Acute bouts of exercise affect tendon structure, with some of the
changes resembling those reported in pathological tendons.
Areas of controversy: Given the variation in study designs, measured parameters
and outcomes, it remains debatable how acute exercise influences overall tendon
properties. There is discrepancy regarding which investigation modality and
settings provide optimal assessment of each parameter.
Growing points: There is a need for greater homogeneity between study designs,
including subject consortium and age, exercise protocols and time frames for
parameter assessing.
*Correspondence address.
Centre for Sports and
Exercise Medicine, Barts
and The London School
of Medicine and
Dentistry, Mile End
Hospital, 275 Bancroft
Road, London E1 4DG,
UK. E-mail: n.maffulli@
qmul.ac.uk
Areas timely for developing research: Innovative methods, measuring each
parameter simultaneously, would allow a greater understanding of how and
when changes occur. This methodology is key to revealing pathological processes
and pathways that alter tendon properties according to various activities. Optimal
tendon properties differ between activities: more compliant tendons are
beneficial for slow stretch shortening cycle (SSC) activities such as
countermovement jumps, whereas stiffer tendons are considered beneficial for
fast SSC movements such as sprinting.
Keywords: tendons/exercise/imaging/biochemistry/structure/physiology
Accepted: December 20, 2011
British Medical Bulletin 2012; 103: 169–202
DOI:10.1093/bmb/ldr052
& The Author 2012. Published by Oxford University Press. All rights reserved.
For permissions, please e-mail: [email protected]
A. Tardioli et al.
Introduction
During exercise and coordinated musculoskeletal movement, tendons are
pivotal in transmitting force from muscle to bone allowing movement.
Historically, the term overuse injury led to research focusing on mediumto long-term effects of exercise on tendons.1 – 3 Tendons are metabolically
active and undergo complex remodelling, which can improve tensile
strength and increased collagen turnover with long-term exercise.3 – 6
Although acute structural changes following bouts of exercise can
stimulate positive adaptations, in some situations these changes may
play a role in the development of tendon injuries,7 illustrating the incomplete understanding of this field. Athletes training on a daily basis
will undertake sessions of varying intensities and duration amid competition, yet there is little evidence correlating exercise, structural changes
and injury progress.
Improved understanding of biochemical markers, sensitive imaging and
mechanical property indicators provide a basis for accurate accounts of
tendon response to acute loading. Recently, with the introduction of ultrasound (US) colour and power Doppler, it has become possible to assess
tendon blood flow changes during and following acute exercise.8 – 10
This review systematically evaluates the immediate and subacute
effects of exercise on tendon structure, providing important information on structural and functional changes that occur with exercise and
the correlation with long-term/overuse injuries.
Methods
Literature search
A comprehensive literature search was performed in October 2011,
using Pubmed, Web of Science, SPORTDiscus, CINAHL and Google
Scholar. A combination of keywords were used to retrieve relevant
literature; ‘tendon’, ‘acute’, ‘exercise’, ‘activity’, ‘tendon stiffness’,
‘Young’s modulus’, ‘Ultrasound’, ‘MRI’, ‘Doppler flow’, ‘Power
Doppler’, ‘neovascularization’, ‘colour/color Doppler’, with no limit
regarding the year of publication.
Study selection
Abstracts were read and screened. Relevant articles from peer-reviewed
journals were retrieved. Bibliographies were hand searched for further
relevant articles. Publications in the following languages were considered:
English, Italian, French, Spanish and Portuguese. It is unclear to what
170
British Medical Bulletin 2012;103
Short-term effects of exercise on tendons
extent in vitro data applies to clinical practice, even so the systematic
approach allowed inclusion of relevant studies to support mechanistic
information and overall understanding of tendon ailments (Fig. 1).4,11 – 14
Fig. 1 Study selection flow diagram.
British Medical Bulletin 2012;103
171
A. Tardioli et al.
Tendon tissue
Tendons are composed predominantly of type I and to a lesser extent
type III collagen, with the remainder composed of a complex extracellular matrix, enclosed in the endotendon alongside blood vessels,
lymphatics and nerves (Fig. 2).15
Tendons are able to withstand considerable forces during physical
activity, adapting to changes in mechanical load over time.4 Positive
tendon plasticity from long-term loading is well documented.4,16 For
example, in the hand the tendons of the extensor and flexor muscles
are long. The flexor muscles are stronger than the extensors, as the
hand requires greater strength for activities such as grasping and catching.17 The tendons of the hand flexors have a greater diameter and
thickness compared with the extensor tendons, with increased tensile
strength and anchoring properties over the extensor tendons.18,19
However, recurring physical activity can lead to overuse injuries.
Tendinopathies are a major cause of morbidity in athletes,20 clinically
characterized by activity-induced pain, local tenderness, swelling21
with subsequent diminished performance. The mechanisms of tendon
injury remain poorly understood, but the characteristics of injured
tendons are well documented histologically, biochemically and at
imaging. These three investigation techniques reveal distorted tendon
appearance, hypercellularity, disorganized collagen bundles, increased
proteoglycan content and neovascularization in chronic tendinopathic
tendons.22,23
Until the relationship between sub-acute, acute and short-term adaptations are scientifically understood and linked with chronic, pathological adaptations, then the explanation of injury mechanism will
remain incomplete and management inadequate.
Results
Biochemical response to exercise
Collagen turnover
Tendon biochemistry is typically described in terms of collagen and
proteoglycan concentrations.3 Long-term exercise and physical training
cause connective tissue remodelling and increased tendon collagen in
both animal and human models.8,24 However, the effect of a single
exercise bout on collagen turnover remains underreported. Some
studies suggest that a single, short bout of exercise does not alter
collagen synthesis25,26 and that more prolonged episodes are required
for turnover to be affected.27
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Short-term effects of exercise on tendons
Fig. 2 Basic tendon structure. Epitenon: connective tissue surrounding each tendon, allows
smooth gliding against adjacent structures. Endotendon: encloses fibres, carrying the
blood vessels, lymphatics and nerves.
When serum markers of collagen degradation [carboxy-terminal telopeptide (ICTP) and carboxy-terminal propeptide (PICP)] are measured
to assess tendon biochemistry, collagen degradation increases immediately post-exercise followed by a significant rise in collagen turnover
for up to 72 h after exercise,27 – 29 and up to 9 days in another study30
(Table 1). Similarly, urinary markers of collagen turnover were
increased for up to 9 days after maximum eccentric contractions of the
knee extensors.31 These studies are limited by their use of serum PICP
and ICTP, as collagen type I is present mainly in bone, and plasma
concentrations may signal turnover in bone as opposed to tendon
tissue.32 Recently, the development of microassays allow accurate,
in vivo collagen turnover rates to be assessed,5,33 as peritendinous
microdialysis probes can monitor in situ PICP and ITCP. Similarly, this
technique showed an initial decrease in Achilles collagen turnover,
followed by a rise 68 h after treadmill running34 and up to 72 h after a
marathon5 in healthy young males. Likewise, collagen synthesis
increased in young women following exercise,35 albeit to a lesser extent
than in males. Although these studies provide important information
on tendon biochemistry, their limitations should be noted. PICP levels
are elevated for at least 3 days following acute exercise,33 and trauma
from a microdialysis fibre insertion itself can cause an increase in PICP
levels.36 Therefore, previous bouts of exercise and/or chronic adaptations may influence subsequent values. A combined in vivo/in vitro
study showed a 1.7-fold increase in tendon collagen synthesis at 6 and
24 h, falling thereafter but remaining elevated at 72 h,37 a longer time
than previously reported.5,38
Exercise increases both collagen degradation and synthesis at defined
time intervals after exercise.37,39 Collagen degradation peaks earlier
(,36 h) than collagen synthesis (up to 72 h), a crucial finding given
British Medical Bulletin 2012;103
173
A. Tardioli et al.
174
Table 1 In vivo biochemical response to exercise: study outline.
Author (year)
Total tendons (total
subjects)
Astrom and
Westlin (1994)43
28
Study outline
Finding
Laser Doppler flowmetry (LDF)
– Passive stretch and isometric contraction led to progressive
decline in LDF
– Microvascular perfusion of Achilles
– Perfusion recorded at rest, during passive stretch and
isometric contraction
– Inverse response; greater tension ¼ reduced perfusion
– Increased tendinous blood flow following muscle contraction
– Blood flow higher in women
Bojsen-Moller
et al. (2006)52
6
PET scanner (radioactive tracer:
[18F]-2-fluoro-2-deoxy-D-glucose)
– Increase in Achilles tendon glucose uptake in response to
loading
– Achilles tendon glucose uptake following low intensity
exercise
– Suggests increase in intratendinous metabolic activity in
response to exercise
– 25 min of intermittent voluntary plantarflexor
contractions
– Boushel et al.
(2000a)44
7
Spatially resolved spectroscopy and isotopic labelling
(133Xe-washout technique)
– Achilles peritendinous blood flow and perfusion
– During graded, dynamic plantarflexion
British Medical Bulletin 2012;103
Boushel et al.
(2000b)45
– Achilles peritendinous blood flow increased 7-fold
– Calf muscle blood flow increased in parallel to tendon flow
– Conclude that peak exercise peritedinous blood flow only
reaches 20% of it maximal capacity
10
Near-infrared spectroscopy (NIRS) (tracer: indocyanine
green) and 133Xe-washout technique
– Achilles peritendinous blood flow during plantarflexion
– NIRS versus 133Xe-washout to compare peritendinous
blood flow (first study)
– Peritendinous blood flow measured using NIRS increased in
response to exercise similar to that determined by 133Xe
washout
– NIRS is a suitable method for determining regional blood flow
in tendinous tissue
British Medical Bulletin 2012;103
Brown et al.
(1997)31
8
Urinary [hydroxyproline (HP) and hydroxylysine (HL)]
– Knee extensor tendons
Brown et al.
(1999)30
– Increased urinary HP and HL recorded on Days 2, 5 and 9
post-exercise
– 50 maximum eccentric contractions
– Conclude that eccentric muscle contractions increase collagen
breakdown into the subacute phase post-exercise
– Indirect indices of muscle and connective tissue
breakdown measured at 1, 2, 5 and 9 days post-exercise
– Non-specific to tendon response
9
Serum (HP and type I collagen)
– Knee extensor tendons
– 2 bouts of 50 concentric and eccentric knee extensions
– No change in serum HP following eccentric or concentric
action up to 9 days post-exercise
– Increased collagen concentration following eccentric exercise
only
– Indirect markers of muscle and collagen breakdown at 1,
3, 7 and 9 days post-exercise
Hannukainen
et al. (2005)51
8
PET scanner
– Glucose uptake increased in response to exercise
– Peritendinous Achilles glucose uptake
– Glucose uptake remained unchanged with increasing intensity
– In response to increasing exercise intensity and duration
– 35 min of cycling at 30, 55 and 75% VO2max
Heinemeier et al.
(2003)34
6
Peritendinous microdialysis and serum—TGF-beta 1,
PICP, ICTP
– Measured before and after treadmill running (1 h and
12 km/h)
Kalliokoski et al.
(2005)54
– Serum TGF-beta 1 increased by 30% in response to exercise
– Increased local production of type I collagen in Achlles in
response to uphill running
– Authors suggest a role for TGF-beta 1 in regulating collagen
type I synthesis
5
Pet scanner
– Patellar and quadriceps tendons
– Glucose uptake/turnover during dynamic extension
exercises
– Glucose increased by 77% in patellar tendon and 106% in
quadriceps tendon
– Tendons are less metabolically active during exercise compared
with muscle
– Suggest tendon glucose uptake regulation is independent of
muscles
175
Continued
Short-term effects of exercise on tendons
– Peritendinous Achilles levels of collagen metabolism
– Peritendinous PICP levels increased 68 h after exercise
Author (year)
Total tendons (total
subjects)
Koskinen et al.
(2004)53
6
Study outline
Finding
Peritendinous microdialysis (MMPs and TIMPs)
– Pro-MMP-9 increased immediately after exercise and elevated
for 3 days
– Achilles tendon
– 1 h of uphill treadmill protocol
– Pro-MMP-2 decreased immediately after exercise but elevated
on Day 3
– Collagen type I degradation products measured before,
immediately after, 1 and 3 days post-exercise
– The inhibitory TIMP elevated for 3 days post-exercise
– Authors conclude that MMPs and therefore protein
degradation are activated in response to exercise
Kristoffersson
et al. (1995)26
7
Serum (PICP, ICTP, calcium, parathyroid hormone and
osteocalcin)
– Study the metabolism of collagen type I in response to
short-term maximal work loads (modified windgate test)
– Raised calcium
– No change in PICP, ICTP, PTH or osteocalcin
– Serum markers non-specific to tendons, limited applicability to
tendon response
– Samples taken before exercise, 5 and 60 min after
exercise
Langberg et al.
(1998)47
10
Isotopic labelling (133Xe tracer)
– Peritendinous Achilles blood flow
– Evaluated before and during 40 min of dynamic
contraction
British Medical Bulletin 2012;103
Langberg et al.
(1999)5
– Blood flow 5 cm proximal to Achilles insertion increased 4-fold
during exercise
– Blood flow 2 cm proximal to insertion increased 2.5-fold
7
Peritendinous microdialysis (PICP, ICTP, PGE2)
– 3-fold increase in PICP at 72 h after exercise
– Achilles tendon, local type I collagen metabolism
– Decrease PICIP immediately after exercise and decrease ICTP
during early recovery
– Levels measured before, immediately after, then at 2 and
72 h following 3 h of running (36 km)
– Conclude that exercise increases the formation of type I
collagen
A. Tardioli et al.
176
Table 1 Continued
British Medical Bulletin 2012;103
Langberg et al.
(1999)39
6
Peritendinous microdialysis (PGE2, TXB2, lactate, glucose,
glycerol)
– Achilles tendon blood flow increased 2-fold
– Achilles tendon metabolism
– Inflammatory activity is accelerated in the peritendinous
region of Achilles following dynamic loading
– 30 min of intermittent static plantarflexion
– 100% increase in PGE2 and TXB2
– Substrates measured at rest, during exercise and 60 min
of rest
– Lipid and carbohydrate metabolism is also increased
– Blood flow also measured by isotopic tracing
Langberg et al.
(1999)48
11
Peritendinous microdialysis (Dextran 70)
– Achilles tendon tissue pressure
– Tissue pressure in the peritendinous area ventral to
tendon
– Negative tissue pressure is generated in the peritendinous
space during exercise
– Negative tissue pressure could lead to fluid shift and be
associated with the increase in peritendinous blood flow
– Pressure measured at rest and during intermittent
isometric calf contractions
Langberg et al.
(1999)46
6
– Exercise induced a 3.4-fold average increase in blood flow
– Achilles tendon peritendinous blood flow
– Valid method to assess the influence of standardized workload
on the physiology and pathophysiology around Achilles
tendon in humans
– Evaluation of blood flow during 30 min of intermittent
static exercise
Langberg et al.
(2000)28
17
Serum (PICP, ICTP, CK)
– Non-specific collagen turnover
– Biomarkers measured before and immediately after a full
marathon
– Markers also measured 1 –6 days post-marathon
– Transient decrease in collagen formation immediately after
marathon
– Rise in collagen synthesis peaked at 72 h and remained
elevated thereafter
– Returned to normal 5 days post-marathon
Continued
177
Short-term effects of exercise on tendons
Isotopic labelling (133Xe)
Author (year)
Total tendons (total
subjects)
Langberg et al.
(2001)50
18
Study outline
Finding
Isotopic labelling (133Xe)
– 50% lower blood flow at rest in the elderly (70 years)
– Achilles tendon
– Peritendinous blood flow increased during exercise 2.5–
3.5-fold across all age groups
– Peritendinous blood flow measured at rest and during
intermittent calf exercises
– Blood flow compared between three age groups (young,
middle-aged and old)
Langberg et al.
(2002)56
– Factors other than blood flow responsible for increased
incidence of tendon injury with age
6
Peritendinous microdialysis (IL-6 concentration)
– Achilles tendon
– The influence of exercise on IL-6 concentration
– Dramatic increase in peritendinous IL-6 following 36-km run in
the hours following exercise
– Increase in serum and muscle levels
– Measured before, then at 2, 24, 48 and 72 h after a
36-km run
– IL-6 measured in the skeletal muscle and serum at the
same time intervals
Langberg et al.
(2002)49
10
Peritendinous microdialysis (bradykinin and adenosine
concentrations)
– Significant rise in bradykinin and adenosine in response to
exercise
– Achilles tendon
– The findings support a role for bradykinin and adenosine in
regulating exercise-induced peritendinous hyperaemia
– 10 min periods of increasing dynamic plantarflexion at
four different loads
British Medical Bulletin 2012;103
Langberg et al.
(2003)55
24 (controls ¼ 6,
COX-2 ¼ 10,
COX ¼ 8)
Peritendinous microdialysis (prostaglandins, COX-1, COX-2
and PGE2)
– PGE2 significantly rose during exercise in the control group
– Achilles tendon
– PGE2 completely inhibited at rest and during exercise in the
group taking unspecific COX inhibitors
– Three separate groups underwent 30 min of
intermittent, isometric plantarflexion
– COX-2 inhibits PGE2 at rest but totally abolished the
exercise-induced increase
– Investigate the role of prostaglandins in exercise-induced
peritendinous blood flow increase
– Concluded that COX-2- specific mechanisms are responsible for
exercise-induced increase in prostaglandin synthesis
A. Tardioli et al.
178
Table 1 Continued
British Medical Bulletin 2012;103
Miller et al.
(2005)37
14 (8 subjects and 6
controls)
Peritendinous microdialysis (IGF-1, IGF and PINP) and
tendon biopsies
– Patellar tendon
– Rise in synthetic collagen rate of 1.7-fold
– Fall in tendon PINP at 72 h after exercise
– Rise in serum CK 24 h after exercise
– 2 groups underwent 1 h of one-legged kicking exercise
(67% max workload)
– Measured at 6, 24, 42 or 48 and 72 h following exercise
Olesen et al.
(2007)36
Skovgaard et al.
(2010)113
12 (6 subjects and 6
controls)
13 (10 controls)
Serum and peritendinous microdialysis (IGF-1, IGFBP, PICP
and ICTP)
– PICP levels were increased in both serum and peritendinous
tissue after 96 h
– Achilles tendon
– Part of the increase due to the trauma from fibre insertion
– Response following 36 km run
– IGFBP-1 increased in both serum and dialysate
– Investigate whether the insertion of microdialysis fibres
causes marker increase
– IGF-1 did not change locally or systemically in either group
PET scanner and isotopic tracer (FLT)
– Treadmill running induced increased uptake of FLT by 21% in
rat Achilles tendons
– Exercise-induced cellular proliferation in rat tendon and
muscle
– Cellular proliferation 3 days before and 48 h after
treadmill exercise
Thorsen et al.
(1996)27
– Coordinated cellular proliferation between muscles and
tendons following exercise
12
Serum (PICP and ICTP)
– Reduced collagen breakdown at 1 h (P , 0.05)
– Serum markers of collagen turnover measured
– Raised PICP and ICTP at 24 and 72 h
– Single bout of brisk walking (50% VO2max) for 90 min
– Data collected before and then 1, 24 and 72 h
post-exercise
Continued
179
Short-term effects of exercise on tendons
– Proliferation measured with PET following radioactive
tracer (FLT)
– Concluded that increased FLT uptake gives at least an
indication of enhanced cellular proliferation of cells in the
Achilles tendon following short-term exercise
A. Tardioli et al.
180
Table 1 Continued
Author (year)
Tofas et al.
(2008)29
Total tendons (total
subjects)
Study outline
Finding
18 (9 subjects and 9
controls)
Serum (HP and HL)
– Serum markers of collagen damage peaked at 48 h and still
elevated at 72 h
– Effect of acute polymetric exercises on indices of
collagen damage
– Measured 7 days before exercise then 24, 48 and 72 h
post-exercise
– Conclude that HP and HL are promising measures of local
tendinous activity
FLT, 30 -[F-18]fluoro-30 deoxythymidine; PGE2, prostaglandin E2; TGF beta 1, transforming growth factor-beta 1; TXB2, thromboxane B2; IGFBP, IGF-binding protein.
British Medical Bulletin 2012;103
Short-term effects of exercise on tendons
repeated, high-intensity training undertaken by elite athletes. It is
possible that, following stress, tendons may require specific recovery
programmes for optimal net anabolic collagen turnover. Insufficient or
ineffective recovery prior to super-compensation may result in net
matrix degeneration, and predispose the tendon to injuries.37,39,40
Additional biochemical response
Tendons were traditionally considered hypovascular, with insufficient
blood supply being central in the injury progression model.41 This traditional concept has been challenged on several occasions15,42 and
current evidence suggests that tendon vascularization is adequate for
their metabolic requirements.43 Innovative techniques allow in vivo assessment of peritendinous blood flow during and after exercise.44 – 46
Blood flow increases 3- to 7-fold during exercise,46,47 controlled predominantly via shifts in peritendinous pressure48 and release of prostaglandins, bradykinin and adenosine.49 Although resting blood flow is
lower in the elderly, exercise induced a significant rise in tendon blood
flow across all ages following activity.50
Glucose uptake in the tendon,51,52 metalloproteases (MMPs) and
tissue inhibitors of metalloproteases (TIMPs)53 increase following exercise further illustrating the metabolic activity of tendons. Indeed, different tendons appear to respond differently to the same exercise bout.
For example, one study showed greater glucose uptake in the quadriceps tendon compared with the patellar tendon following a standardized exercise bout.54 Exercise also influences peritendinous lactate,
prostaglandin-E2, thromboxane-B2 and IL-6 turnover.39,55,56 Of particular interest is the level of peritendinous IL-6, which follows a
similar trend to collagen turnover following exercise. Cytokines and
prostaglandins are believed to play a crucial role in tendon collagen
synthesis and degradation during and shortly after mechanical
loading.40
These findings demonstrate the capacity of tendons to acutely
respond to loading at the protein and cellular levels. To identify
whether short-term, metabolic responses affect tendon pathology,
further research should focus on metabolic activity at regular, standardized post-exercise time intervals. Insufficient recovery may be pivotal
in altering the ‘collagen synthesis-breakdown cycle’ leading to net
catabolism and tendinopathy development.
Biomechanical response to exercise
Historically, the studies on the effects of exercise on tensile properties
were based on in vitro animal investigations.57,58 Recent advances in
British Medical Bulletin 2012;103
181
A. Tardioli et al.
US practice allow for non-invasive, in vivo assessment of fascicle movement and cross-sectional area of human tendons.4 US is currently the
best method to assess tendon mechanics, providing real-time data,
larger fidelity in viewing tendons at a relatively lower cost, as indicated
in 20 of the 23 biomechanical studies identified (Table 2). Mechanical
properties of tendons adapt to long-term exercise;1 for example, the
tendon of vastus lateralis was more compliant in male sprinters compared with control subjects.59 In addition, tendon properties may vary
according to the dominance of a particular limb: for example, patellar
tendon stiffness was greater in the lead leg of badminton and fencing
athletes.60 Serial US assessments may be used to monitor the effectiveness of training programmes designed to improve mechanical properties
of tendons, such as stiffness (elasticity) and strength.
All these studies were planned to assess tendon behaviour under
different situations and conditions. Achilles tendon stiffness varies
during graded, voluntary plantarflexion,61,62 with greater stiffness
reported at higher loads.63 Although studies have shown a linear
force –length relationship of the Achilles,64 – 66 the association is in fact
a positive curvilinear one, given the ‘toe’ region phenomenon when
tendon’s properties differ at low force levels.67
When the mechanical properties of the distal portion of the tendon
of tibialis anterior were assessed, stress increased with increasing isometric force65,68 although it remains unclear whether values obtained
during isometric plantarflexion can be applied to functional activities
(i.e. running).
Tendon loading results in the storage of passive elastic energy, which
is returned during recoil. Recoil of the distal portion of the quadriceps
tendon increases with increasing intensities of drop jump exercises,69
and stored elastic energy increases during varying phases of jumping in
the Achilles,70 gastrocnemius medialis71 and patellar tendons.72
Other studies with methodological differences found that exercise
intensity and duration affect mechanical behaviour. Patellar tendon
stiffness was 77% greater following three short (3 –4 s) compared with
three long (10–12 s) maximal ramped isometric contractions,73 and
compliance of the knee extensor tendons increased more after 50 repetitions of isometric leg presses compared with 100 consecutive drop
jumps.74 Also, short duration (60 s), of static plantarflexion, reduced
the stiffness of the Achilles tendon for up to 30 min,75 and 10 min of
passive ankle dorsiflexion decreased the stiffness and hysteresis of the
Achilles tendon.76 Other studies included in this review do not support
the view that acute biomechanical adaptations result from exercise.
The stiffness and fatigue properties of the Achilles tendon were not
affected by high-intensity hopping exercises,77 and submaximal
fatiguing protocols did not acutely alter the mechanical properties of
182
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British Medical Bulletin 2012;103
Table 2 Studies outlining the acute effects of exercise on biomechanical properties of tendons.
Author (year)
Total tendons
(total subjects)
Couppe et al.
(2008)60
7
Investigation modality and study outline
Findings
MRI and US
– Habitual loading leading to increased PT size and mechanical
properties
– Patellar tendon (PT)
– Fencing and badminton athletes
– For a given force, stress was less on the lead leg
– Properties compared between lead and non-lead leg
during isometric contractions
Finni et al.
(2000)72
4
Optic fibre
– Achilles and PTs
– Tendon forces during submaximal squats and counter
movements
– Tendons shown to undergo stretch-shortening cycle and possess
potential for elastic energy storage
– Acute interaction between muscle and tendon may utilize elastic
energy storage which is generated at variable activity levels
– Two-legged jumps on a force plate and one-legged jump
on a sledge plate
Fukashiro et al.
(1995)70
1
Implanted transducer
– Achilles tendon
– (i) Maximal vertical jump from squat (33 cm); (ii) maximal
vertical jump from erect (40 cm) and (iii) repetitive
hopping (7 cm)
Giddings et al.
(2000)85
– 23% elastic storage during squat jump
– 17% elastic storage in countermovement jump
– 34% elastic storage during hopping
Cineradiography and force plate
– Maximum loads occurred late in the stance phase
– Achilles tendon
– 70% of the stance phase during walking and 60% of the stance
phase during running
– Measure calcaneal stresses during walking and running
Continued
183
Short-term effects of exercise on tendons
– Elastic behaviour of one tendon during jumping
– The Achilles stored variable percentages of elastic energy during
different phases
Author (year)
Total tendons
(total subjects)
Ishikawa et al.
(2003)69
8
Investigation modality and study outline
Findings
US
– Fascicle length decreased and recoil of tendinous tissue increased
with increasing rebound intensities
– Vastus lateralis tendon (distal)
– Interaction between tendinous tissue and muscle fasicle
– Measured during varying intensity stretch-shortening
cycles; single leg squat vs. drop jumps from constant
height
Ito et al. (1998)68
9
US
– Tendon stiffness increased with force
– Tibialis anterior tendon
– Increasing force ¼ shortened fasicle length, increased pennation
angle and elongation
– Fasicle length, pennation angle and elongation measured
gradually during isometric dorsiflexion torque
Kay et al. (2009)75
– At higher rebound intensities, fascicle controlled during the
breaking phase in such a manner that effective recoil of the
tendon takes place during final push-off phase
– Conclude that US is valid in determining stiffness and Young’s
modulus for human tendons
16
US and motion analysis
– Achilles tendon
– MVICs significantly reduced peak concentric moment and Achilles
tendon stiffness
– Decrease in Achilles tendon stiffness remained 30 min later
– Effect of maximal voluntary isometric contractions (MVICs)
on mechanics
– Stretch protocol caused no significant change in any measure
– (i) Six 8 s MVICs performed and (ii) three 60 s static
plantarflexor stretches
British Medical Bulletin 2012;103
Kubo et al.
(2001)76
7
US
– Stretching produced no significant change in MVC
– Medial gastrocnemius tendon
– Stretching decreased tendon stiffness and hysteresis
– Influence of ramp isometric plantarflexion on viscoelastic
properties up to the maximum voluntary contraction
(MVC)
– Stretching decreased tendon viscosity but increased elasticity
– 10-min passive ankle dorsiflexion
A. Tardioli et al.
184
Table 2 Continued
British Medical Bulletin 2012;103
Kubo et al.
(2005)74
8
US
– Tendon compliance increased after longer duration contractions
– Knee extensor tendons
– No change in tendon elongation at any force in response to DJ
– Effect of repetitive drop jumps (DJ) and isometric leg
presses (LP) on properties
– Each subject performed 100 reps of DJ and 50 reps of LP
for 10 s with 10 s relaxation
Kurokawa et al.
(2003)71
8
US and electromyography
– Tendon of gastrocnemius medialis
– Behavior of fascicles and tendon structure during
maximal-effort counter movement jumping
Lichtwark et al.
(2005)64
– Energy is rapidly released during the upward phase
– Interaction between fascicles and tendinous structures essential in
generation of higher joint power
10
US
– Force –length relationship of the whole tendon is linear
– Achilles tendon
– Prolonged hoping may cause tendon damage
– Determine Achilles stress and strain during one-legged
hopping and the contribution of elastic recoil to
mechanical energy changes
– Conclude that elastic properties of tendons contribute
significantly to the mechanical work but individual variation
varies the tendon’s energy storage capacity
US
– No change in strain or elongation following each fatiguing task
– Gastrocnemius medialis tendon
– No change in tendon compliance following exercise
14
– Effects of submaximal fatiguing protocols on the
compliance of tendons
– Isometric maximal voluntary plantarflexion contractions
(MVC) before and after two fatiguing protocols
Continued
185
Short-term effects of exercise on tendons
Mademli et al.
(2006)78
– Elastic energy stores in the tendinous structures during the latter
downward phase
Author (year)
Mademli and
Arampatzis
(2008)79
Total tendons
(total subjects)
Investigation modality and study outline
Findings
26 (12
young þ 14
old)
US
– No change in mechanical properties following ‘long-lasting’ static
or cyclic loading
– Gastrocnemius tendon
– Age-related effects of submaximal loading on tendon
properties
– No difference between age groups
– Subjects performed isometric plantarflexions before and
after fatiguing task
Maganaris and
Paul (1999)65
5
US and MRI
– Tibialis anterior tendon
– Effect of increasing contraction intensities on mechanical
properties of the tendon (less highly stressed tendon,
compared with (AT)
Maganaris and
Paul (2002)63
British Medical Bulletin 2012;103
Magnusson et al.
(2001)66
– Tendon force and stress increased linearly as a function of
displacement and strain, respectively
– Under physiological loading, tendon stiffness and Young’s
modulus are in agreement with in vitro studies
6
US
– Achilles stiffness increased during graded plantarflexion
– Gastrocnemius segment of Achilles tendon
– Values fall within the range of in vitro studies
– Change in tensile properties during isometric
plantarflexion, force calculated from the moment
generated about the joint
– Study indicates that gastrocnemius tendon provides 6% of total
work during walking
US and MRI
– Tendon stiffness and Young’s modulus increased according to
graded flexion
– Greater contributions in more active exercise (i.e. running)
5
– Achilles tendon (proximal and distal segments)
– Load – displacement and stress –strain characteristics
– Each subject carried out graded, 10 s isometric
plantarflexions
– Exceeding measurements previously reported in vivo but similar
to in vitro values
A. Tardioli et al.
186
Table 2 Continued
British Medical Bulletin 2012;103
Magnusson et al.
(2003)114
5
US
– Achilles tendon
– Assess and compare mechanical characteristics of the
Achilles tendon and its aponeurosis during isometric
contractions
Muramatsu et al.
(2001)115
US
– Load-strain characteristics of tendon during graded
isometric plantarflexion
– Comparison between proximal and distal regions of the
tendon aponeurosis
– Suggest separate functional roles for these structures
– No difference in strain characteristics between Achilles tendon
and its aponeurosis
– No difference between proximal and distal regions of the
aponeurosis
– Conclude: Achilles tendon is homogeneously stretched along its
length during the contraction of medial gastrocnemius
38
US
– Distal portion of the Achilles had the greatest cross-sectional area
– Achilles tendon
– No correlation between Achilles cross-sectional area and its
‘calculated’ stiffness
– Determine whether geometric properties of the tendon is
the main determinant of its elasticity, measured from 3
separate points along the tendon
– Conclude that stiffer tendons are not necessarily thicker.
Therefore, tendon geometric properties may not be the major
determinant of its elasticity
9
US
– PT
– Effects of contraction duration on strain properties (short
3 –4 s, long 10 –12 s)
– Subjects performed 3 short and 3 long maximal isometric
contractions
– Strain and excursion lower for short duration contractions
compared with long duration
– Tendon stiffness was 77% greater for short duration compared
with long
– Conclude that contraction duration significantly affects tendon
strain and stiffness at all levels of force
Continued
187
Short-term effects of exercise on tendons
– Tendon stiffness calculated from subjects developing
maximum voluntary isometric plantarflexion (MVIP)
Pearson et al.
(2007)73
– Free Achilles tendon demonstrates greater strain compared with
the distal aponeurosis during isometric contraction
7
– Achilles tendon
Muraoka et al.
(2004)116
– At a common force, deformation and length greater in the
tendon compared with aponeurosis
A. Tardioli et al.
188
Table 2 Continued
Author (year)
Total tendons
(total subjects)
Peltonen et al.
(2010)77
10
Investigation modality and study outline
Findings
US and MRI
– Tendon stiffness not affected by increasing isometric contractions
(measured before and after exercise)
– Achilles tendon
– Effects of a single bout of high impact hoping exercise on
tendon stiffness
– Subjects performed two-legged hopping exercises (range,
1150 –2600 jumps)
– Maximum tendon force decreased during graded MVCs
– Conclude: mechanical fatigue is not reached after a single bout of
exhaustive high-impact exercise in the Achilles tendon
– Measured at several isometric contractions up to 100%
MVC
Rosager et al.
(2002)62
10 (5 runners
and 5 controls)
US and MRI
– Achilles tendon
– Comparison of load –displacement and stress –strain
characteristics of the triceps surae tendon between
runners and non-runners
– Subjects performed graded maximal voluntary
plantarflexion exercises
Ullrich et al.
(2009)80
– Tendon cross-sectional area was greater in runners compared with
non-runners
– No difference in tensile force between runners and non-runners
– Plantarflexion moment was similar in runners and non-runners
– Conclude; tendon stiffness and maximal strain did not vary
between the two groups
12
US
British Medical Bulletin 2012;103
– Vastus lateralis tendon
– Effects of (i) submaximal sustained and (ii) maximal
repetitive contractions on compliance of vastus lateralis
tendon
– Subjects performed 3 MVC of the knee extensors before
and after the two fatiguing protocols
– No change in elongation and strain of the tendon before and
after fatiguing protocols
– Conclude that vastus lateralis tendon (and its aponeurosis)
compliance was not affected by long-lasting static mechanical
loading nor long-lasting cyclic mechanical loading
Short-term effects of exercise on tendons
the tendon of gastrocnemius medialis78,79 or of the vastus lateralis.80
Load –displacement and stress – strain characteristics of the Achilles
tendon did not differ between runners and non-runners during graded
plantarflexion efforts.62
The significance of these findings lies with the concept that compliant
tendons are advantageous in some activities, whereas stiff tendons are
beneficial in others.67 Stretching a compliant tendon results in elastic
storage which is passively returned during recoil increasing the contribution of elastic strain to movement allowing for greater performance.81 For
example, compliant knee extensor tendons in sprinters help develop
higher force during the stance phase in which the foot contacts the
ground,59 and a compliant Achilles tendon will provide substantially
more passive elastic energy compared with non-compliant tendons.
When joint position and control are advantageous, stiffer tendons
provide greater control than compliant tendons when crossing the joint.67
Stretching, performed prior to exercise, is shown to reduce stiffness76,82 and increase range of motion,83 thus reducing the risk of
injury. However, current evidence suggests that stretching has no true
effect on athletic performance or injury risk.84
While this review found that the mechanical properties of tendons
are affected by activity duration and intensity.68,74,85 the functional
implications of acute tensile loading remains unclear. Variations in
methodology, tendons assessed, subject numbers and exercise protocols
provide the main obstacle to comparing results between studies.
Further research is needed to understand the different loads at which
mechanical properties are affected. If mechanical properties vary with
exercise, training programmes could be tailored to work tendons at
specific, optimal loads.
Radiological response to exercise
Musculoskeletal imaging is widely accessible for the assessment of
tendon injuries in athletes and allows recognition of true pathology.
Magnetic resonance imaging (MRI) and US are the most commonly
used imaging modalities (Table 3), and the interpreter requires a
wealth of literature evidence along with clinical expertise to accurately
report images.
Magnetic resonance imaging
MRI is used to assess and grade tendon injuries.86 Long-term exercise
leads to a number of positive MRI findings without associated clinical
British Medical Bulletin 2012;103
189
Author
Number of tendons (total
subjects)
Boesen et al.
(2006)8
42 (21)
Imaging modality/study outline
Findings
Colour Doppler US
– Increased tendon Doppler flow in asymptomatic individuals
following exercise
– Achilles tendon
– Evaluate vascular activity after repeated loading
in symptomatic and asymptomatic tendons
– 10 subjects ran 5 km and 11 performed
heavy-load eccentric exercise
Boesen et al.
(2006)106
– Eccentric exercise does not extinguish the flow after one training
session in patients with chronic AT
– Presence of Doppler activity in the Achilles does not per se
indicate disease
92 (46)
Colour Doppler US
– Achilles tendon
– Evaluation of vascular activity in direct response
to badminton match
– High incidence of Doppler flow in elite badminton players at
baseline (84%)
– Doppler flow was present in at least one tendon of each player
after the match
– Grades of Doppler flow increased in response to exercise
Cahoy et al.
(1996)90
10 (5)
MRI
– ‘Rotator cuff’ tendons (non-specific)
– Examine tendon appearance following
strenuous exercise using ‘Biodex system 2’
objective protocols
– Tendon signal remained unchanged from pre-exercise through
24 h post-exercise
– MRI scanning may take place after a practice session without an
increased risk of false positive
– Imaging before, immediately after then at 8
and 24 hr after exercise
Cook et al. (2005)10
34 (17)
British Medical Bulletin 2012;103
Colour Doppler US
– Median vessel length increased after volleyball match
– PT
– Significant increase in tendon vascularity induced by exercise
(P ¼ 0.001)
– Known abnormal tendons examined before
and after volleyball match
– Tendon vascularity assessed
– Moderate exercise significantly enhances the detection of tendon
blood flow
– Assessment of neovascularization should be carried out following
exercise
A. Tardioli et al.
190
Table 3 Acute, in vivo changes at imaging following exercise.
British Medical Bulletin 2012;103
Drongelen et al.
(2007)97
42 (42)
Grey-scale US
– Long head biceps
– Tendons examined before and after wheelchair
basketball or quad rugby
Fahlstrom and
Alfredson (2010)98
Fredberg et al.
(2007)93
– Mean AP diameter increased from 4.60 to 4.82 mm, but not
significant (P ¼ 0.178)
– Echogenicity ratio decreased following exercise (P ¼ 0.038)
– Positive correlation between playing time and tendon diameter
(P ¼ 0.004)
36 (18)
Grey-scale and colour Doppler US
– Mean tendon thickness decreased after 1 h of match play
– Achilles tendon
– Greater blood flow after than before the match
– Tendons examined immediately before and
after 1 h of floor-ball match play
– All painful tendons had structural abnormalities on US
Grey-scale US
– Mean tendon AP diameter increased by 0.13 mm
– Achilles tendon
– Change in thickness not statistically different
20 (10)
– 150 repeated ankle plantarflexions in 1.5 min
Grigg et al. (2009)99 22 (11)
Grey-scale US
– Both loading conditions decreased Achilles tendon thickness
– Achilles tendon
– Eccentric induced greater decrease compared with concentric
loading (20.21 vs. 20.05 P0.05)
– Effects of isolated eccentric and concentric calf
exercise on sagittal thickness
Koenig et al.
(2010)111
– Tendon recovery over 24 h was comparable between both
loading groups
92 (46)
Colour Doppler US
– Anterior knee tendons (quadriceps, patellar
and tibial insertion of patellar)
– Evaluation of vascular activity in direct response
to badminton match
– High prevalence of tendon pain and Doppler activity before and
after the match
– Badminton match did not result in increased intratendinous flow
– CF increased in the dominant leg and at the tibial tuberosity
after play
– Colour fraction (CF) calculated using computer
software
191
Continued
Short-term effects of exercise on tendons
– Measured before, immediately after and 3, 6,
12 and 24 h post-exercise
Author
Number of tendons (total
subjects)
Lohman et al.
(2001)87
38 (19 subjects, 19 controls)
Imaging modality/study outline
Findings
MRI
– Main limitation: no pre-marathon data, limiting conclusions
– Foot (non-tendon specific)
– MRI abnormalities found in marathon runners and asymptomatic
physically active individuals. No significant changes between
both groups
– MR examination within 3 h of completing
full-length marathon
Shalabi et al.
(2004)88
44 (22)
MRI
– Achilles tendon
– Evaluate tendon response to acute strength
training in chronic Achilles tendinosis
– Eccentric and concentric loading of Achilles result in increased
tendon volume
– Increased intratendinous signal in symptomatic and
asymptomatic tendons after exercise (P , 0.001)
– Volume change may be caused by increased water content and/or
vascular hyperaemia following strength training
Terslev et al.
(2001)102
13 (7)
Grey-scale and colour Doppler US
– PT
– 7 players examined before and after basketball
match
– Poor presentation limits strength and high probability of type II
study error
– No sound evidence to demonstrate the acute effects of exercise
on these tendons
– No correlation between symptoms and US changes
Freund et al.
(2011)89
103 (53) (73 initial runners
and 20 non-finishers)
MRI
British Medical Bulletin 2012;103
– Achilles tendon
– Evaluate the response of tendons to a
marathon or half-marathon
– Wide range of experience between runners
(novices to very experienced)
– Three images performed. (i) point of
enrolment; (ii) end of training and (iii) within
72 h of race
– Achilles diameter in asymptomatic German runners greater than
reported in symptomatic American population at baseline
– Tendon diameter was not affected by marathon running (up to
72 h after)
– Mean volume of tendon lesions increased after the marathon
– No new lesions are expected following exercise
A. Tardioli et al.
192
Table 3 Continued
Short-term effects of exercise on tendons
findings.87,88 However, imaging is often performed to assess acute injuries, clinicians must be aware of both habitual and abnormal changes
following exercise (Fig. 2).
One study showed that the Achilles tendon structure was acutely
altered by activity in symptomatic and asymptomatic individuals following standardized eccentric exercises.88 Tendon volume and intratendinous signal increased, indicating a significant change in water
content and blood flow.88 In another study, runners with intratendinous lesions at baseline developed increased volume after a marathon
or half-marathon.89
Conversely, other studies fail to elicit a statistically significant response, with no change in the structure of foot tendons between
runners and controls after the runners completed a marathon.87
Another study showed that the diameter of the Achilles tendon was not
affected by a marathon, and no new lesions were seen after activity.89
Also, the structure of the rotator cuff tendons was not altered by exercise immediately or at 8 and 24 h after the end of the exercise bout.90
Disparities in study design and populations limit comparability of
results between studies. One study examined tendinopathic Achilles’,
one included normal and tendinopathic tendons, another assessed
asymptomatic rotator cuff tendons (non-specific) and another assessed
foot structures, without focusing on a specific tendon.
The normal MRI anatomy of tendons is variable,91 providing
inherent limitations when comparing studies. The search undertaken
for the present review retrieved four studies (Table 3), and remains
unclear whether exercise induces acute changes in the MRI appearance.
Therefore, imaging performed shortly after exercise may be misinterpreted and misdiagnosed. Advances in the quality of diagnostic US
reduces the need for the more expensive and resource intensive MRI
technique. Future research should assess tendon volume and signal
changes following exercise, clarifying the difference between pathological findings and expected changes after exercise.
Ultrasound
US is increasingly used to assess and diagnose tendon pathology in
sporting injuries.16,92,93 Clinicians using US should be aware of typical
and abnormal changes that occur in response to acute exercise.
Acute thickness change
Thickened tendons are associated with tendinopathy and morbidity,16,94 yet tendons can become thicker as a habitual response to longstanding exercise.4,41,94 – 96
British Medical Bulletin 2012;103
193
A. Tardioli et al.
Fig. 3 Bar chart illustrating the change in US diameter from the studies. Note the studies
reporting an increase in tendon diameter were not found to be significant.
Tendon diameter was not significantly affected by acute, shortduration mechanical loading93 or by longer, high-intensity activity.97 A
small sample in the former and the different tendons between studies
(Achilles93 vs. long head of biceps97) limits the validity of the combined
results. Interestingly, the biceps tendon study found a positive correlation between ‘play time’ and increased tendon diameter, suggesting
that the duration of exercise may play an important role.
Other studies, however, showed a decrease in tendon diameter
following exercise. One hour of high-intensity exercie98 and another
programme involving isolated concentric/eccentric exercises99 significantly reduced AP tendon diameter (Fig. 3). From the included studies,
there is greater evidence that tendon diameter decreases immediately
after exercise, although the significance of this on tendon pathology is
unknown.
Grey-scale ultrasonographic changes/echogenicity
Normal tendons are described as having homogeneous appearance on
US (Fig. 4a). Structures containing more fluid, fat or other less
194
British Medical Bulletin 2012;103
Short-term effects of exercise on tendons
Fig. 4 Ultrasound appearance of the Achilles tendon illustrating three main parameters. (a)
Normal homogenous appearance of the Achilles tendon (thin arrows). Tendon fibres are
regular throughout with no hypoechoic areas. The tendon inserts into the calcaneus (light
arrow). (b) Abnormal grey-scale appearance of the Achilles tendon. Localised thickenng,
hypoechoic areas (arrows) and irregular fibre composition (circled). (c) Abnormal Achilles
tendon demonstrating florid Doppler flow/neovascularization (circled) with hypoechoic
lesions (arrows) and gross thickening.
echo-reflective tissue have a hypoechoic appearance (Fig. 4b), similar to
changes associated with tendinopathy.97 Echogenic tendon changes are
common in athletes,94,100 but the correlation between echogenic
changes and symptoms, including pain, is poorly understood.
Hypoechoic areas are essentially constant findings in tendinopathy, yet
hypoechoic areas are seen in the tendons of asymptomatic
individuals.100,101
Terslev et al.102 assessed the patellar tendons of 18 basketball players
to determine whether echogenicity was affected by a match. Although
new changes in echo pattern were reported after the match, only 7 of
the initial 18 players were re-examined after the match, failing to
provide power to infer that the match was directly responsible for the
echoic changes. Another study showed that the tendon of the long
head of the biceps was significantly more hypoechoic following exercise,97 and concluded that this probably represented acute tendon
oedema, similar to that seen in the early stages of tendon pathology.103
Evidence of acute echoic changes following exercise remains scarce,
and our understanding of how this correlates with tendon pathology
remains hypothetical.
Acute Doppler flow response to exercise
Athletes may exhibit a florid Doppler flow in tendons
(Fig. 3c).4,9,23,104,105 There is a correlation between tendon Doppler
flow and pain9,105 – 107 as well as Doppler flow and echogenic
changes,9 although no conclusions can be made that changes are a
direct result of acute exercise. Blood flow itself is not the unique cause
of pain108,109 but exercise-induced neovascularization23,110 probably
plays a pivotal role in the development of tendinopathies and their
associated symptoms. Cook et al.10 assessed Doppler flow in the
British Medical Bulletin 2012;103
195
A. Tardioli et al.
patellar tendons of 17 volleyball players with established neovascularization before and after a match and found a significant increase immediately after the match. The authors suggest a standardized exercise
protocol before US examination, increasing tendon vascularity and optimizing Doppler detection.105
Koening et al.111 measured Doppler flow in the patellar tendons of
46 elite badminton players before and after a match. Of these 92
tendons, 92% had Doppler flow before and after the match, but the
match did not result in significantly increased intratendinous flow.
These unexpected findings were attributed to the large training loads
of elite athletes, in whom tendons are more or less always in a metabolically active state.111 However, in a further study by the same authors,
Doppler flow in the Achilles tendon increased significantly after the
match in the same group of badminton players,106 challenging the
theory that tendons’ activity remains fixed during rigorous training in
athletes. It is possible that different tendons respond in a different
fashion based on the functional demands of that activity (swinging,
jumping, running, etc.).
Increased Doppler flow following exercise is also reported in the
Achilles tendon8,106,112 and Doppler flow was increased in both symptomatic and asymptomatic individuals following different exercise protocols.106 The same authors used a five-point grading system to report
an increase in Achilles Doppler flow in 46 elite badminton players following a match. Colour Doppler flow was present in 83% of tendons
at baseline (Grades 1 –4), covering mid-tendon, pre-insertional and calcaneal regions of the Achilles tendon. Following the match, all players
had colour Doppler flow in one or both Achilles tendons. The extent
of Doppler flow in the pre-insertional area was significantly increased
after the match in the dominant and non-dominant foot.106 Fahlstrom
et al. assessed 36 tendons before and after a ‘floor-ball’ match using US
and colour Doppler. Neovascularization was present in 7 of 36
tendons before and after the match, 6 of these 7 tendons showed significantly greater flow.98 Similar to the patellar tendon,10 loading the
Achilles tendon induces increased intratendinous Doppler flow, and
may be a normal physiological response.106 Given these findings, it is
proposed that US assessment of tendons is carried out after exercise
where visualization of vascularity is optimized.10,105
Further studies are needed to investigate the sonographic response of
normal tendons to exercise, including a wider range of tendons.
Furthermore, painful tendons which initially do not show Doppler
activity may require a loading programme to optimize vascularity
assessment.8,10 Standardized exercise protocols to be carried out prior
to tendon imaging are needed.
196
British Medical Bulletin 2012;103
Short-term effects of exercise on tendons
Conclusions
Our understanding of the acute response of tendons to exercise remains
in the preliminary phase with evidence lacking in certain areas. Current
knowledge relies on studies that were limited to measuring one or two
variables, and also relies heavily on data from a limited selection of
tendons, mainly the Achilles and patellar tendons. There is little
research integrating biochemical, biomechanical and imaging findings
of exercise on tendons, likely due to the practicalities of such research
which would be difficult to overcome. However, such integration is imperative to understand the acute effects of exercise on tendons and its
contribution to pathology. Combining techniques such as microdialysis, tissue biopsy sampling, US and MRI in future research may be key
to understanding the underlying mechanisms that ultimately result in
tendon injury. Enhanced knowledge and understanding of injury
mechanism is imperative for the development of effective treatment
and prevention strategies.
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