209 Full
209 Full
209 Full
Br J Sports Med: first published as 10.1136/bjsports-2015-095215 on 25 September 2015. Downloaded from http://bjsm.bmj.com/ on June 11, 2021 by guest. Protected by copyright.
Tendon neuroplastic training: changing the way
we think about tendon rehabilitation: a narrative
review
Ebonie Rio,1,2 Dawson Kidgell,3 G Lorimer Moseley,4 Jamie Gaida,1,5,6
Sean Docking,1,2 Craig Purdam,7 Jill Cook1,2
▸ Additional material is ABSTRACT will ultimately affect tendon loading and motor
published online only. To view Tendinopathy can be resistant to treatment and often performance. Therefore, it is logical to explore the
please visit the journal online
(http://dx.doi.org/10.1136/ recurs, implying that current treatment approaches are corticospinal pathway in people with tendinopathy.
bjsports-2015-095215). suboptimal. Rehabilitation programmes that have been Given the high incidence of bilateral tendinopa-
1 successful in terms of pain reduction and return to sport thy1 and bilateral pathology with predominantly
Department of Physiotherapy,
School of Primary Health Care, outcomes usually include strength training. Muscle unilateral load in animal2 and human studies,3 it is
Monash University, Melbourne, activation can induce analgesia, improving self-efficacy also important to consider the corticospinal control
Victoria, Australia
2
associated with reducing one’s own pain. Furthermore, of the non-painful side in tendinopathy. A frequent
The Australian Centre for strength training is beneficial for tendon matrix structure, and frustrating phenomenon is the clinical presen-
Research into Injury in Sport
and its Prevention, Ballarat muscle properties and limb biomechanics. However, tation of the previously unaffected side following
Federation University, Victoria, current tendon rehabilitation may not adequately address rehabilitation. These observations pose several clin-
Australia the corticospinal control of the muscle, which may result ical questions: what are the differences in motor
3
Department of Rehabilitation, in altered control of muscle recruitment and the control between those people with tendinopathy
Nutrition and Sport, School of
consequent tendon load, and this may contribute to and those without (that may predispose people to
Allied Health, La Trobe
University, Melbourne, recalcitrance or symptom recurrence. Outcomes of tendinopathy or may be adaptations)? Are there
Victoria, Australia interest include the effect of strength training on tendon side-to-side differences associated with unilateral
4
Sansom Institute for Health pain, corticospinal excitability and short interval cortical tendinopathy? How well does our current rehabili-
Research, University of South inhibition. The aims of this concept paper are to: (1) tation therapy address these issues of motor
Australia & Pain, Adelaide,
South Australia, Australia
review what is known about changes to the primary control?
5
Department of Physiotherapy, motor cortex and motor control in tendinopathy, (2)
University of Canberra, Bruce, identify the parameters shown to induce neuroplasticity MOTOR CONTROL IN PEOPLE WITH AND
Australian Capital Territory, in strength training and (3) align these principles with WITHOUT TENDINOPATHY
Australia tendon rehabilitation loading protocols to introduce a
6 In tendon research, muscle strength, usually repre-
University of Canberra
Research Institute for Sport combination approach termed as tendon neuroplastic sented by maximal voluntary contraction (MVC), is
and Exercise, Australia training. Strength training is a powerful modulator of the far more often evaluated than is motor control.
7
Department of Physical central nervous system. In particular, corticospinal inputs Interestingly, there is no consistent pattern of
Therapies, Australian Institute are essential for motor unit recruitment and activation; strength or performance change (either increase or
of Sport, Bruce, Australian
Capital Territory, Australia
however, specific strength training parameters are decrease) in those tendons that have been studied
important for neuroplasticity. Strength training that is (or the contralateral limb) and this may conflict
Correspondence to externally paced and akin to a skilled movement task with the clinical perception that pain is likely to
Ebonie Rio, 4 Hardy Crescent, has been shown to not only reduce tendon pain, but result in strength loss due to disuse or willingness
Heathmont VIC 3135,
modulate excitatory and inhibitory control of the muscle to protect the injured part consciously or subcon-
Australia:
Ebonie.rio@monash.edu and therefore, potentially tendon load. An improved sciously. For example, people with rotator cuff
understanding of the methods that maximise the (RC) tendinopathy have been shown to be 15%
Accepted 5 September 2015 opportunity for neuroplasticity may be an important stronger in measures of abduction on their asymp-
Published Online First progression in how we prescribe exercise-based tomatic side than controls (and comparable in
25 September 2015
rehabilitation in tendinopathy for pain modulation and strength to controls on their symptomatic side),4
potentially restoration of the corticospinal control of the and this has also been seen in lateral epicondylal-
muscle-tendon complex. gia.5 Athletes with patellar tendinopathy (PT, also
termed jumper’s knee) have been shown to be
better jumpers than athletes without jumper’s
knee6 7; however, several studies report less
Open access INTRODUCTION strength on the symptomatic side than in controls
Scan to access more
free content
The clinical outcomes of treatment of tendinopathy (see Heales et al8 for review). It is also reported
vary—there is currently no single effective treat- that full strength is not recovered after surgery for
ment. Unimodal interventions aimed solely at per- Achilles tendinopathy.9 There is no convincing
ipheral tissue, in this case the tendon, are unlikely association between strength deficit and presence of
to address complex corticospinal and neuromuscu- tendinopathy, as demonstrated by several studies.8
lar adaptations associated with persistent pain. In People with PT displayed greater cortical inhib-
To cite: Rio E, Kidgell D, this paper, the term corticospinal control of the ition in their quadriceps responses10 than healthy
Moseley GL, et al. Br J muscle will refer to motor unit activation as a individuals.11 Increased cortical inhibition has been
Sports Med 2016;50: result of excitatory and inhibitory corticospinal shown to be associated with phasic (occurring in
209–215. inputs onto the spinal motor neuron pool, which phases/intermittent) nociceptive stimuli,12 which
Rio E, et al. Br J Sports Med 2016;50:209–215. doi:10.1136/bjsports-2015-095215 1 of 8
Review
Br J Sports Med: first published as 10.1136/bjsports-2015-095215 on 25 September 2015. Downloaded from http://bjsm.bmj.com/ on June 11, 2021 by guest. Protected by copyright.
describes tendon pain is consistently linked with loading and across patient and control groups clearly points to an imbalance
therefore, often phasic rather than tonic (sustained) for many between the excitatory and inhibitory influences over muscle
tendons. While there was increased cortical inhibition altering activation around the painful tendon. There may be several
motor drive in PT, there was also greater corticospinal excitabil- mechanisms that underpin these problems, not least changes in
ity (CSE) than in controls inferring differences in the balance of the response profile of clusters of neurons in M1, but the exact
excitability and inhibition of motor control as compared with mechanisms remain to be untangled. Nonetheless, the func-
healthy controls (Rio et al, in press). It may be that strength tional result seems consistent with a protective adaptation that
changes still represent a decrease from that individual’s potential reduces the mechanical demands placed on the tendon, that is,
performance. an apparently protective adaptation.
A recent systematic review by Heales et al8 on the sensory Jumping and landing mechanics will be influenced by motor
and motor deficits of the non-injured side of patients with uni- control changes that include both peripheral and central contri-
lateral tendon pain included one study on the patellar tendon butions to lower limb activation. People with patellar tendon
and one study on the Achilles tendon; however, there were 18 abnormality ( pathologically observable on ultrasound) have
studies on the upper limb tendons. There is clearly a paucity of demonstrated landing patterns different from those of controls
literature investigating lower limb sensory and motor changes in and importantly, have less variability in movement than healthy
tendinopathy. The included lower limb studies measured arch controls.28 Movement variability is thought to minimise load
height in PT13 and Achilles tendon structure with imaging.14 It accumulation in a specific region and reduced variability may be
is not clear how arch height and imaging changes may relate to observed in, for example, reduced coefficient of variation in
sensory or motor changes; thus, the sensory or motor changes knee joint angles during a landing task.29 The invariable motor
in lower limb tendinopathy require further investigation. This pattern implies that corticospinal control is altered in some way
bias towards upper limb studies was paralleled by a recent sys- and may be due to protective strategies underpinned by evalu-
tematic review on complex regional pain syndrome, which only ative processes relating to the consequence or meaning of the
identified suitable data from upper extremity studies.15 It is pos- motor task.30 In the case of patellar tendon abnormality, invari-
sible that differences in functional reorganisation in the primary able motor patterns may reflect a strategy to avoid pain during
somatosensory (and/or primary motor cortex (M1)) cortices jumping (consequence) as well as the competing desire for
following upper limb versus lower limb injury may exist that optimal performance (meaning). In fact, better jumping ability
limit the extrapolation of upper limb findings to the lower limb. has been shown to be a risk factor for developing PT31 and
Given that the predominant role of the upper limb musculature indeed, people with PT are better jumpers or at least as good as
relates to position and control of the hand in space, and that the those without—termed the ‘jumper’s knee paradox’.6 7 32
hand is well represented on the somatosensory cortex and M1, Less variability has been observed in asymptomatic controls
injury to upper limb regions may have manifestations associated who demonstrate a protective postural strategy when they
with chronicity that are different from those in the lower limb. expect their back to hurt,33 and people with recurrent back pain
There appears to be a bias towards investigations of upper limb demonstrate a protective strategy even when they are pain
conditions. free.34 Moreover, a reduction in normal variability of postural
The cross-sectional design of all studies that have investigated adjustments has been observed during experimentally induced
motor control in tendinopathy makes it difficult to infer causal- pain, and failure to reinstate normal variability has been pro-
ity and the potential impact of handedness or hand-use profiles posed as a possible risk for recurrence.30 Such findings raise the
(especially in upper limb studies).16–18 That is, there is a more possibility that an invariable motor pattern observed in PT may
complex relationship at play: talented jumpers are more likely reflect a system less adaptable to environmental perturbations—
to play in positions that require more jumping (eg, in volleyball, an undesirable state.35 Indeed, movement variability has been
as an outside hitter rather than a setter);19 thus, such partici- proposed as an important feature in actually preventing injury.36
pants may be more vulnerable to tendon pain in their dominant Though the predicted goal of adopting a different motor
limb, which is likely to have been stronger than their other one strategy is protection, non-resolution of the strategy may in fact
to begin with. These factors will also affect measures of strength increase the likelihood of symptom recurrence.30 Given the high
and the stimulus response characteristics of primary motor recurrence rate of tendinopathy, it is pertinent to consider that
cortex (M1) cells. Furthermore, maximal strength performance there may be non-resolution of motor strategies even in cur-
data are vulnerable to cognitive and motivational factors.20 21 rently asymptomatic people with a history of tendon pain, or
More importantly, maximum strength measures may not reflect tendon pathology, that predisposes them to symptoms or
the complex interaction between excitatory and inhibitory influ- symptom recurrence. This outcome may also reflect the compet-
ences on the motor command that occur during tasks. ing desires for optimal performance and tissue protection. This
Indices of maximum strength may not provide enough detail adds complexity to the design and implementation of rehabilita-
about muscle-tendon loading at submaximal levels, nor have the tion, as the strategy (movement pattern) adopted will reflect
ability to grade muscle recruitment22 or appropriately timed competing desires of performance and protection, particularly if
patterns of activation according to the required task, especially there has been no change to inputs (of which nociception is
in a painful state (eg, see Hodges and Richardson,23 and only one). To provide a clinical example, the presence of a posi-
Wadsworth and Bullock-Saxton24). Each of these scenarios have tive ‘culture’ of PT in jumping sports, such as volleyball where
significant implications for function and load attenuation.25 playing with tendon pain is common (and may reinforce a
Transcranial magnetic stimulation (TMS) studies have shown concept that pain during activity does not equate to tissue
that athletes with PT have greater M1 excitability than pain-free damage), will probably serve to maintain the motor control
jumping athletes, as reflected in larger evoked muscle responses strategy. These contextual factors are likely to further influence
in the quadriceps (rectus femoris; Rio et al,10 in press). As the experience of pain,37 and will vary depending on the envir-
stated, athletes with PT also have greater cortical inhibition than onment and one’s own experiences.
healthy controls have.11 26 27 That the investigation of these Cross-sectional studies do not allow elucidation of whether
issues involves identical loading and contextual environment tendon pathology or the presence of tendon pain precedes
2 of 8 Rio E, et al. Br J Sports Med 2016;50:209–215. doi:10.1136/bjsports-2015-095215
Review
Br J Sports Med: first published as 10.1136/bjsports-2015-095215 on 25 September 2015. Downloaded from http://bjsm.bmj.com/ on June 11, 2021 by guest. Protected by copyright.
changes in motor control. That pain will often be accompanied baseball pitchers)3 and unilaterally loaded animal models that
by altered motor output would be predicted on the basis that demonstrate bilateral pathology2 implicate systemic or nervous
both pain and motor output can be effective at protecting us system involvement in tendinopathy. The interhemispheric con-
from bodily threat. A common finding in studies of motor nections and potential for modulation at the spinal cord level
control during pain is altered corticospinal drive to the motor are both potential avenues for bilateral changes outside of bilat-
neuron/muscle. However, this phenomenon of greater CSE has eral loading that have not been as yet investigated.
also been observed during testing that was non-painful, in It is possible that the other side may display differences in
people with PT as compared with activity-matched controls and response to unilateral nociception (or insult) similar to what is
people with other anterior knee pain (Rio et al, accepted). observed in injury such as stroke. The adaptive response seen
Furthermore, there were no differences between groups for following stroke includes increased inhibition on the affected
activity, muscle strength (measured by maximal voluntary iso- side and increased CSE to the unaffected limb.42 Furthermore,
metric contraction torque of the quadriceps), muscle activation there is actually increased interhemispheric inhibition from the
(represented by surface electromyography) or measures of non-affected hemisphere to the lesioned hemisphere that further
motor neuron activation (maximal femoral nerve stimulation); increases the inhibition on the affected side during activation of
so it seems plausible that the increase in CSE was associated the unaffected limb.42 This perhaps has a biological advantage
with the PT regardless of the fact that there was no pain during to improve efficiency of the unaffected side; however, this
testing. It is possible that their net motor drive to the quadriceps remains a challenge in rehabilitation (as the affected side has sig-
muscle group is unaltered (or even that they may not be as good nificant inhibition and is further increased during activation of
as they could be); however, controlled activation and the motor the unaffected limb).
strategy may be affected. This also implies the motor task still To investigate the unaffected side in people with PT, 13
has potential ‘consequence’ and ‘meaning’ in the absence of jumping athletes (6 control participants, 7 with unilateral PT)
nociception, which fits with the invariable and abnormal were recruited (Rio, unpublished data available as an online
landing strategy observed in people with tendon pathology. supplementary material). Participants were tested bilaterally
Current tendon rehabilitation may fail to adequately address with TMS including their active motor threshold and a stimulus
the multitude of contributing factors to altered motor control, response curve as well as short interval cortical inhibition (SICI)
which would include not only muscle strength and tendon cap- using rectus femoris as the target muscle. When compared with
acity, but corticospinal control encompassing excitability and healthy, activity-matched controls, preliminary data in athletes
inhibition as well as belief systems about pain and contextual with PT demonstrate hyperexcitability on their affected side,
factors. supporting previous research (Rio et al, unpublished, available
as an online supplementary material) and also displayed mark-
Motor control changes may be bilateral edly increased cortical inhibition (n=4 affected side SICI ratio
The lack of consistent abnormalities in muscle strength on the 17.12%, n=6 controls 58.78%). This motor control strategy
patient’s affected leg may simply reflect similar abnormalities may be likened to a novice driver controlling the speed of their
being present on the contralateral limb. Heales et al8 reported car with one foot on the brake and one on the accelerator.
that the contralateral asymptomatic side was weaker than con- Interestingly, the contralateral pathway controlling the
trols in upper limb tendinopathy, though abduction in those unaffected side appears less excitable than both the affected side
with RC tendinopathy was an exception and no data were (similar to that observed in stroke) and controls, and also dis-
reported for the lower limb. Interestingly, data from low back plays increased cortical inhibition (n=4 unaffected side 19.13%;
pain studies are also variable with some reporting both hypoac- where lower SICI percentage ratio represents greater cortical
tivity and others reporting hyperactivity, depending on the inhibition). These preliminary findings appear to replicate the
muscles and tasks investigated (see Hodges and Moseley38 for findings of unilateral stroke that affects the M1, in particular the
review). Strength deficits persist following surgery and rehabili- plausibility of greater interhemispheric inhibition and involve-
tation in unilateral Achilles tendinopathy; however, the ment of bilateral changes. However, the sample size is small and
side-to-side strength difference was relatively low (7.2–8.8%) warrants further investigation with greater numbers. It does,
and may actually reflect a bilateral motor control deficit.9 nevertheless, highlight the danger of using the unaffected side as
However, while the direction of change (increases or decreases a control in studies of motor control, excitability or inhibition
in muscle performance) is not consistent, it does appear that a in people with tendinopathy. This also requires further evalu-
change in motor control may occur bilaterally. ation as the clinical implications are considerable—strength
Regardless of whether motor control changes are a cause of training in the affected limb may continue to drive inhibition to
pain or epiphenomena, changes to motor control may not just the unaffected limb unless we can improve our understanding of
be bilateral but system wide. There is an increasing body of evi- techniques that modulate excess inhibition.
dence that multiple sites are frequently affected due to complex Given the propensity for lower limb activities to be bilateral
intrinsic and extrinsic factors, and contralateral pathology and/ and symmetrical for efficiency (ambulation, jumping, etc), the
or the development of symptoms is common. That is, once changes in the unaffected side may be an attempt to achieve
tendon pain (or pathology) is established at one site, there motor control homoeostasis in a system trying to protect a
appears to be the potential for increased risk of tendinopathy region. That is, there are combined and perhaps competing
elsewhere. Notwithstanding systemic risk factors that predispose demands of protecting a vulnerable or potentially vulnerable
tendinopathy, such as diabetes, elevated cholesterol and genetic tendon while still producing torques sufficient for optimal per-
factors (eg, the COL5A1 genotype in isolation39 or in combin- formance. This may be argued for many tendinopathies not just
ation),40 there may be other considerations, including an in athletes, but in people involved in manual labour or any
increase in global sympathetic drive.41 While it is likely that outcome-dependent task.
loading is similar for both legs and bilaterality of pathology The contralateral motor control changes may also contribute
(and/or pain) may be, therefore, somewhat expected, data from to or explain the high injury rate of the contralateral tendon fol-
the upper limb with markedly different use profiles (such as lowing rehabilitation. That is, loading patterns in the
Rio E, et al. Br J Sports Med 2016;50:209–215. doi:10.1136/bjsports-2015-095215 3 of 8
Review
Br J Sports Med: first published as 10.1136/bjsports-2015-095215 on 25 September 2015. Downloaded from http://bjsm.bmj.com/ on June 11, 2021 by guest. Protected by copyright.
contralateral limb are likely to be different as corticospinal drive activation and leaving people vulnerable to recurrence of
of the unaffected side is altered. This provides support for a symptoms.
rehabilitative strategy that targets the corticospinal control of People can and do recover in terms of pain and function
both sides; however, these strategies may need to be carefully despite tendon pathology remaining unchanged on clinical
considered. Strategies that modulate inhibition on the affected imaging.50 One plausible explanation for this, at a tissue level, is
side as well as pain, such as isometric muscle contractions in that the tendon may structurally compensate in the area around
PT,10 should be evaluated for their potential effect on interhe- the pathological lesion. That is, the volume of structurally intact
mispheric inhibition and inhibition of the ipsilateral M1. tissue increases as an adaptive response.51 This tendon may be
Rehabilitation that is capable of modulating pain and inhibition thicker but potentially amenable to improvements in mechanical
of both M1 may yield important advances in tendon strength51 through graded rehabilitation that would also alter
management. muscle properties. The reverse is also observed, however, where
patients can have symptoms without demonstrable structural
THE KEY QUESTION IS WHAT HAPPENS FIRST? pathology and reminds us that there is a disconnect between
There are two theories about the relationship between pain and structure and pain (see Rio et al52). Non-painful motor activa-
changes in muscle control (see Hodges and Moseley38 for tion would also improve self-efficacy; so there are a number of
review), and neither is supported unequivocally by the litera- potential mechanisms linking rehabilitation (in particular
ture. They propose that either changes in muscle activity cause strength training) to improvements in symptoms. However,
pain (sometimes termed pain-spasm-pain model or vicious cycle given the clinical observation that ‘once a tendon, always a
of pain in the pain literature) or that changes in muscle activity tendon’ reflects the strong tendency for symptom recurrence,
serve to protect the area by limiting movement (the pain adapta- there is clearly room for improvement in our strategic approach.
tion model).43 Given the differences in motor control observed across tendino-
Experimental pain studies that demonstrate transient changes pathies, how well does current rehabilitation address motor
to motor control after a transient nociceptive stimulus,44–46 as control?
well as studies on a number of chronic conditions provide
support for the pain adaptation model.43 The definitive study RESISTANCE TRAINING AND MOTOR CONTROL
that studies motor control before the onset of pain remains Muscle activation involves activation of broad cortical and sub-
elusive. cortical regions.53 54 Self-paced resistance training describes a
Hyperexcitability of the quadriceps in athletes with PT has process without external timing cues (such as visual or audi-
been correlated with length of time of symptoms (Rio, unpub- tory). In the clinical setting, an example of self-paced resistance/
lished data available as an online supplementary material) and strength training may be where a patient is advised to complete
changes in infraspinatus excitability in people with RC tendino- three sets of 10 contractions lifting a certain weight—it is
pathy were correlated with chronicity.47 This does not exclude without advice about the timing of the contraction (eccentric
the possibility that aberrant motor control precedes the first and concentric phase) nor are there timing cues, such as a
onset of tendinopathy but provides a strong rationale that metronome sound, to provide structure to the timing of the
changes in motor control occur in response to nociceptive contraction. Studies that have used external pacing, for
barrage. The potential for unilateral nociceptive input to drive example, with a metronome where the individual would con-
motor control changes bilaterally (or possibly even system wide) tract concentrically and eccentrically to the sound of the metro-
underlines the importance of improving our understanding of nome and complete these phases exactly as prescribed or follow
nociception-motor interactions,48 particularly in a condition of a visual cue to match the pace of the contraction phases, have
chronic nociception where the nociceptive driver is unknown. demonstrated increases in excitability in both skill (visuomotor
The pain adaptation model proposes that agonist activity is tracking)55 or short-term resistance training.56–58 Leung et al58
reduced and the antagonist activity is increased with pain.43 investigated the effects on excitability and inhibition of a single
This may be the case in PT as there were no differences in bout of visuomotor tracking compared with self-paced resistance
MVC between athletes with PT and controls (Rio et al, training and metronome-based resistance training. They found
accepted). However, in a separate study, following isometric that both skilled training and metronome-paced resistance train-
exercise that reduced their pain, the MVC of the quadriceps of ing, but not self-paced resistance training, increased excitability
athletes with PT increased by 18.7%, implying their agonist and released inhibition in both the trained limb and in the
activity (the quadriceps) was in fact inhibited (reduced) prior to untrained limb. This has implications for tendinopathy rehabili-
isometric exercise.10 The hamstrings that serve as the antago- tation as both CSE and inhibition have been shown to be differ-
nists have not been measured. Most testing is completed in the ent compared with controls.
laboratory with a single joint movement for simplicity, for
example, leg extension; however, agonists and antagonists CURRENT TENDON REHABILITATION AND PROPOSED
would change during a more complex movement such as a CONCEPT
counter movement jump. Current rehabilitation aims to restore tendon and muscle prop-
The threat to tissue (as far as the brain is concerned) may erties using exercise with a variety of paradigms. There is evi-
remain even after pain reduction and return to sport, as tendon dence for the efficacy of eccentric-only contractions59–64 and
may not have ‘healed’ (many consider tendinopathy to be failed heavy slow resistance (involving both a concentric and eccentric
healing; see Cook and Purdam49 for review). In this context, component)65 in improving pain and function in Achilles and
there may be ongoing monitoring and persistent changes to cor- PT. Protocols that include strength training (load) appear to
ticospinal control of muscle (to protect the tendon) as the M1 provide the greatest stimulus for the tendon and muscle.
and its projections may consider it to be vulnerable. However, deficits in muscle performance have been shown to
Alternatively, the motor control changes that occur in tendino- persist following surgical intervention plus rehabilitation or
pathy may not spontaneously resolve or normalise following rehabilitation alone for tendinopathy, despite positive clinical
recovery, thus indicating rehabilitation may not address motor outcomes.9 66 Current prescription of tendinopathy
4 of 8 Rio E, et al. Br J Sports Med 2016;50:209–215. doi:10.1136/bjsports-2015-095215
Review
Br J Sports Med: first published as 10.1136/bjsports-2015-095215 on 25 September 2015. Downloaded from http://bjsm.bmj.com/ on June 11, 2021 by guest. Protected by copyright.
rehabilitation is best described as self-paced where patients are material). Two strategies were trialled, either isometric or iso-
provided exercises with guidance of repetitions, sets and load tonic quadriceps muscle contractions, using TNT (the combin-
(all of these are variable and no gold standard exists) but, ation of heavy strength training and externally pacing) due to a
importantly, without external pacing (either visual or auditory). lack of efficacious in-season loading options and both active
Given the high recurrence rate of tendinopathy and persistent treatments. This had a clinical basis to answer the questions:
motor changes following rehabilitation,66 it is possible that which programme may reduce pain immediately in-season and,
current rehabilitation fails to restore corticospinal control of the was there any difference between them over a 4-week trial? As
muscle-tendon complex(s). both groups were externally paced with the training, it was
Rehabilitation protocols are historically directed at local hypothesised they would both improve in excitability and inhibi-
tissue adaptation (muscle hypertrophy and tendon) and there tory control. However, one protocol may be better for analgesia
has been little, if any, focus on modulating corticospinal and this may also affect control, particularly cortical inhibition.
control. It is possible that these approaches, therefore, only A subgroup of 9 athletes completed the corticospinal testing
address some of the neuromuscular and muscle-tendon before and after the 4-week TNT intervention (that recruited 29
changes in tendinopathy. Furthermore, passive unimodel treat- athletes) and 1 of the athletes completed weekly testing (figure
ments, such as injections, are unlikely to address local or 2). An online supplementary material is available with the
central deficits such as tendon capacity, muscle strength across method and full data set.
the kinetic chain and these issues of excitability and inhibition Isometric exercise provided greater immediate analgesia (Rio
(figure 1A–D). et al, submitted) and both protocols reduced pain significantly
Externally paced resistance training, such as with the use of a over the 4-week trial (van Ark et al, submitted). There were no
metronome, is capable of inducing ipsilateral and contralateral differences between groups after 4 weeks. A case study demon-
changes to the excitability and inhibition in healthy partici- strates that there are changes in excitability over the course of
pants.11 57 67–69 To investigate this concept in a PT model, a 4 weeks and week 4 most closely represents normal CSE in
protocol was developed that used externally paced strength jumping athletes without PT.
training, termed tendon neuroplastic training (TNT) (protocol Testing showed that TNT, using either isometric or isotonic
available in Rio et al, submitted and online supplementary muscle contractions, changed inhibition ( p=0.008; figure 3).
Figure 1 Summary of different approaches of tendon rehabilitation, and effects on strength and motor control. (A) Passive intervention fails to
address strength and capacity of the tendon or muscle as load is required to stimulate these tissues; this leads to an inability to perform the task
and an undesired outcome on the left. An example may be an injection into the tendon aimed at restoring tendon structure. Simultaneously, motor
control has not been addressed; thus, the drive to the muscle may be unchanged and the outcome remains undesirable. (B) This likely describes
most current clinical rehabilitative approaches that focus on strength. The local tissue has probably improved in its characteristics (tendon
mechanical properties, muscle strength); however, the drive to the muscle has not been addressed due to the nature of self-paced resistance
training; thus, the outcome may still be undesired ( perhaps in terms of recurrence). (C) In this example, the focus may be purely on trying to alter
the biomechanics or motor control with repetition and feedback about the task (eg, proprioception exercises). This not only has been shown to have
poor integration into the sporting environment, it also has not addressed the tissue capacity. Therefore, the local feedback to the central nervous
system is likely to maintain the motor control pattern as an ongoing protective or adaptive strategy. (D) The concept of tendon neuroplastic training
includes using strength training to address the tendon as load is the only stimulus shown to promote the matrix. Furthermore, strength training
improves muscle architecture. In this example, the external pacing of strength training also serves to address cortical muscle control in an attempt to
improve the muscle recruitment pattern and therefore, also tendon load.
Rio E, et al. Br J Sports Med 2016;50:209–215. doi:10.1136/bjsports-2015-095215 5 of 8
Review
Br J Sports Med: first published as 10.1136/bjsports-2015-095215 on 25 September 2015. Downloaded from http://bjsm.bmj.com/ on June 11, 2021 by guest. Protected by copyright.
Figure 2 Individual weekly response
to tendon neuroplastic training
(isometric protocol). Mean±SEM MEP
amplitude (note error bars are too
small to be seen; MEP, motor evoked
potential).
Preliminary data for the individuals and group responses are CONCLUSION AND CLINICAL IMPLICATIONS
provided. The values are a percentage representing cortical Self-paced strength training targeted to improving muscle archi-
inhibition of the quadriceps where normative values (for those tecture describes the parameters of most clinical rehabilitation
without PT) are 50–70%.11 26 All athletes improved to be programmes for tendinopathy. These may not adequately
within the normal range following the intervention; hence, this address the differences in excitability and inhibition that has
represents a physiologically important change. There were dif- been observed in PT and may be a feature of other tendinopa-
ferences between the isometric and isotonic group (figure 3); thies. The alterations to corticospinal control of muscle may
however, clinical implications are limited based on small sample manifest as a different motor strategy (for protection); however,
size. Furthermore, a larger study that compared self-paced with this could contribute to ongoing morbidity or vulnerability to
externally paced would elucidate if the effects are associated symptom recurrence. Movement variability appears an import-
with a reduction in nociception or the use of external pacing or ant factor in chronicity, yet it is not commonly considered in
a combination. Data in healthy participants would support the musculoskeletal pain conditions and may be relevant even if
use of external pacing over self-pacing in targeting the M1 and nociceptive input is absent. Aberrant tendon load from altered
given the nociception-motor interactions,48 external pacing may motor control may be transmitted to tendon causing perpetu-
augment changes. ation of nociceptive input. However, the altered pattern also
Figure 3 Individual cortical inhibition responses to tendon neuroplastic training by muscle contraction type. Isometric: p=0.06, isotonic: p=0.25,
TNT group including both paradigms: p=0.008. Each individual participant’s data are provided with diamond denoting preintervention and triangle
denoting postintervention for that person.
6 of 8 Rio E, et al. Br J Sports Med 2016;50:209–215. doi:10.1136/bjsports-2015-095215
Review
Br J Sports Med: first published as 10.1136/bjsports-2015-095215 on 25 September 2015. Downloaded from http://bjsm.bmj.com/ on June 11, 2021 by guest. Protected by copyright.
appears to serve the desire for performance because many Ethics approval MUREC.
studies demonstrate that people with tendinopathy display Provenance and peer review Not commissioned; externally peer reviewed.
superior strength or performance. Current rehabilitation for Data sharing statement Unpublished data that contribute to the concept
tendinopathy focuses on strength training because it stimulates provided in this review are available as an online supplementary material. This
the physiological adaptation of muscle and tendon. However, includes pilot testing as well as further information about the intervention for
strength training that is externally paced has also been shown to clinicians and researchers.
be able to modulate tendon pain and corticospinal control of Open Access This is an Open Access article distributed in accordance with the
muscle. The concept of TNT incorporates loading that has been Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which
permits others to distribute, remix, adapt, build upon this work non-commercially,
shown to be efficacious both in the short and longer term for and license their derivative works on different terms, provided the original work is
tendinopathy (4 weeks; Rio et al, in submission), in a pain-free properly cited and the use is non-commercial. See: http://creativecommons.org/
protocol which is tolerated by athletes in a competitive environ- licenses/by-nc/4.0/
ment, as well as those parameters that promote changes to corti-
cospinal muscle control. The current programme may induce REFERENCES
change by reducing tendon pain. As clinicians and scientists, it is 1 Cook JL, Khan KM, Harcourt PR, et al. Patellar tendon ultrasonography in
important that we progress our understanding of the mechan- asymptomatic active athletes reveals hypoechoic regions: a study of 320 tendons.
isms behind improvements (or lack thereof ) to improve patient Victorian Institute of Sport Tendon Study Group. Clin J Sport Med 1998;8:73–7.
2 Andersson G, Forsgren S, Scott A, et al. Tenocyte hypercellularity and vascular
outcomes in tendinopathy. This will need to also consider proliferation in a rabbit model of tendinopathy: contralateral effects suggest
rehabilitation that addresses the unaffected side, which appears the involvement of central neuronal mechanisms. Br J Sports Med 2011;45:
to display motor adaptations. How belief systems may impact 399–406.
the prognosis of people with tendinopathy also needs to be 3 Miniaci A, Mascia AT, Salonen DC, et al. Magnetic resonance imaging of the
shoulder in asymptomatic professional baseball pitchers. Am J Sports Med
explored.
2002;30:66–73.
4 Brox JI, Roe C, Saugen E, et al. Isometric abduction muscle activation in patients
with rotator tendinosis of the shoulder. Arch Phys Med Rehabil 1997;78:1260–7.
5 Bisset LM, Russell T, Bradley S, et al. Bilateral sensorimotor abnormalities in
What are the findings? unilateral lateral epicondylalgia. Arch Phys Med Rehabil 2006;87:490–5.
6 Lian O, Engebretsen L, Ovrebo RV, et al. Characteristics of the leg extensors in male
volleyball players with jumper’s knee. Am J Sports Med 1996;24:380–5.
▸ Tendinopathy may be associated with changes in motor 7 Lian O, Refsnes PE, Engebretsen L, et al. Performance characteristics of volleyball
control; these changes may be bilateral and persistent players with patellar tendinopathy. Am J Sports Med 2003;31:408–13.
despite rehabilitation. 8 Heales LJ, Lim EC, Hodges PW, et al. Sensory and motor deficits exist on the
non-injured side of patients with unilateral tendon pain and disability—implications
▸ Current rehabilitation may not adequately address motor for central nervous system involvement: a systematic review with meta-analysis.
control issues as self-paced strength training (the mainstay Br J Sports Med 2014;48:1400–6.
of the treatment) does not alter corticospinal drive to the 9 Ohberg L, Lorentzon R, Alfredson H. Good clinical results but persisting side-to-side
muscle—this may contribute to recalcitrance and recurrence differences in calf muscle strength after surgical treatment of chronic Achilles
of tendinopathy. tendinosis: a 5-year follow-up. Scand J Med Sci Sports 2001;11:207–12.
10 Rio E, Kidgell D, Purdam C, et al. Isometric exercise induces analgesia and reduces
▸ Tendon neuroplastic training proposes a concept of inhibition in patellar tendinopathy. Br J Sports Med 2015;49:1277–83.
strength-based loading that is an important stimulus for 11 Weier AT, Pearce AJ, Kidgell DJ. Strength training reduces intracortical inhibition.
tendon and muscle, but with strategies known to optimise Acta Physiol 2012;206:109–19.
neuroplasticity of the motor cortex and drive to the muscle. 12 Dubé JA, Mercier C. Effect of pain and pain expectation on primary motor cortex
excitability. Clin Neurophysiol 2011;122:2318–23.
It needs to be tested in a wide range of anatomical 13 Crossley KM, Thancanamootoo K, Metcalf BR, et al. Clinical features of patellar
locations as it is unclear whether findings for the patellar tendinopathy and their implications for rehabilitation. J Orthop Res
tendon are applicable to all tendinopathies. 2007;25:1164–75.
14 Grigg NL, Wearing SC, Smeathers JE. Achilles tendinopathy has an aberrant strain
response to eccentric exercise. Med Sci Sports Exerc 2012;44:12–17.
15 Di Pietro F, McAuley JH, Parkitny L, et al. Primary motor cortex function in complex
regional pain syndrome: a systematic review and meta-analysis. J Pain
Twitter Follow Ebonie Rio at @tendonpain and James Gaida at @tendonresearch 2013;14:1270–88.
Acknowledgements Ms Kay Copeland is acknowledged for her suggestion of the 16 Klöppel S, van Eimeren T, Glauche V, et al. The effect of handedness on cortical
term ‘Tendon neuroplastic training’ for the concept. JC was supported by the motor activation during simple bilateral movements. Neuroimage 2007;34:
Australian Centre for Research into Sports Injury and its Prevention, which is one of 274–80.
the International Research Centres for Prevention of Injury and Protection of Athlete 17 Bäumer T, Dammann E, Bock F, et al. Laterality of interhemispheric inhibition
Health supported by the International Olympic Committee (IOC). JC is a NHMRC depends on handedness. Exp Brain Res 2007;180:195–203.
practitioner fellow (ID 1 058493). GLM is supported by an Australian National 18 Volkmann J, Schnitzler A, Witte OW, et al. Handedness and asymmetry of hand
Health and Medical Research Council Principal Research Fellowship (NHMRC ID representation in human motor cortex. J Neurophysiol 1998;79:2149–54.
1061279). ER is supported by an Australian Postgraduate Award. ER, SD and CP are 19 Bahr MA, Bahr R. Jump frequency may contribute to risk of jumper’s knee: a study
adjunct research fellows of the Australian Centre for Research into Sports Injury and of interindividual and sex differences in a total of 11,943 jumps video recorded
its Prevention. during training and matches in young elite volleyball players. Br J Sports Med
2014;48:1322–6.
Contributors All authors were involved in study planning and design, including 20 Kroll W. Test reliability and errors of measurement at several levels of absolute
the intervention. ER and DK were responsible for data collection that contributed to isometric strength. Res Q 1970;41:155–63.
the paper and this is available in the online supplementary material. SD designed 21 Peacock B, Westers T, Walsh S, et al. Feedback and maximum voluntary contraction.
the figures in the paper. ER was the main author, and responsible for the concept Ergonomics 1981;24:223–8.
and primary preparation of the manuscript. All authors were involved in manuscript 22 St Clair Gibson A, Lambert ML, Noakes TD. Neural control of force output during
editing and preparation. maximal and submaximal exercise. Sports Med 2001;31:637–50.
Funding The Australian Institute of Sport Clinical Research Fund 23 Hodges PW, Richardson CA. Altered trunk muscle recruitment in people with low
(ACTRN12613000871741) supported the RCT for which data are provided within back pain with upper limb movement at different speeds. Arch Phys Med Rehabil
this manuscript. 1999;80:1005–12.
24 Wadsworth DJ, Bullock-Saxton JE. Recruitment patterns of the scapular rotator
Competing interests None declared.
muscles in freestyle swimmers with subacromial impingement. Int J Sports Med
Patient consent Obtained. 1997;18:618–24.
Br J Sports Med: first published as 10.1136/bjsports-2015-095215 on 25 September 2015. Downloaded from http://bjsm.bmj.com/ on June 11, 2021 by guest. Protected by copyright.
25 Seitz AL, McClure PW, Finucane S, et al. Mechanisms of rotator cuff tendinopathy: 49 Cook JL, Purdam CR. Is tendon pathology a continuum? A pathology model to
intrinsic, extrinsic, or both? Clin Biomech (Bristol, Avon) 2011;26:1–12. explain the clinical presentation of load-induced tendinopathy. Br J Sports Med
26 Goodwill AM, Pearce AJ, Kidgell DJ. Corticomotor plasticity following unilateral 2009;43:409–16.
strength training. Muscle Nerve 2012;46:384–93. 50 Drew BT, Smith TO, Littlewood C, et al. Do structural changes (eg, collagen/matrix)
27 Rantalainen T, Weier A, Leung M, et al. Short-interval intracortical inhibition is not explain the response to therapeutic exercises in tendinopathy: a systematic review.
affected by varying visual feedback in an isometric task in biceps brachii muscle. Br J Sports Med 2014;48:966–72.
Front Hum Neurosci 2013;7:68. 51 Docking SI, Cook J. Pathological tendons maintain sufficient aligned fibrillar
28 Edwards S, Steele JR, McGhee DE, et al. Landing strategies of athletes with an structure on ultrasound tissue characterization (UTC). Scand J Med Sci Sports
asymptomatic patellar tendon abnormality. Med Sci Sports Exerc 2010;42:2072–80. 2015.
29 James CR, Dufek JS, Bates BT. Effects of injury proneness and task difficulty on joint 52 Rio E, Moseley L, Purdam C, et al. The pain of tendinopathy: physiological or
kinetic variability. Med Sci Sports Exerc 2000;32:1833–44. pathophysiological? Sports Med 2014;44:9–23.
30 Moseley GL, Hodges PW. Reduced variability of postural strategy prevents 53 Cohen LG, Ziemann U, Chen R, et al. Studies of neuroplasticity with transcranial
normalization of motor changes induced by back pain: a risk factor for chronic magnetic stimulation. J Clin Neurophysiol 1998;15:305–24.
trouble? Behav Neurosci 2006;120:474–6. 54 Gerloff C, Cohen LG, Floeter MK, et al. Inhibitory influence of the ipsilateral motor
31 Visnes H, Aandahl HA, Bahr R. Jumper’s knee paradox—jumping ability is a risk cortex on responses to stimulation of the human cortex and pyramidal tract.
factor for developing jumper’s knee: a 5-year prospective study. Br J Sports Med J Physiol 1998;510(Pt 1):249–59.
2013;47:503–7. 55 Ackerley SJ, Stinear CM, Byblow WD. Promoting use-dependent plasticity with
32 Siegmund JA, Huxel KC, Swanik CB. Compensatory mechanisms in basketball externally-paced training. Clin Neurophysiol 2011;122:2462–8.
players with jumper’s knee. J Sport Rehabil 2008;17:358–71. 56 Kidgell DJ, Pearce AJ. Corticospinal properties following short-term
33 Moseley GL, Nicholas MK, Hodges PW. Does anticipation of back pain predispose strength training of an intrinsic hand muscle. Hum Mov Sci 2010;29:
to back trouble? Brain 2004;127(Pt 10):2339–47. 631–41.
34 Hodges PW, Richardson CA. Inefficient muscular stabilization of the lumbar spine 57 Kidgell DJ, Stokes MA, Castricum TJ, et al. Neurophysiological responses after
associated with low back pain. A motor control evaluation of transversus short-term strength training of the biceps brachii muscle. J Strength Cond Res
abdominis. Spine (Phila Pa 1976) 1996;21:2640–50. 2010;24:3123–32.
35 Stergiou N, Decker LM. Human movement variability, nonlinear dynamics, and 58 Leung M, Rantalainen T, Teo WP, et al. Motor cortex excitability is not
pathology: is there a connection? Hum Mov Sci 2011;30:869–88. differentially modulated following skill and strength training. Neuroscience
36 Bartlett R, Wheat J, Robins M. Is movement variability important for sports 2015;305:99–108.
biomechanists? Sports Biomech 2007;6:224–43. 59 Frohm A, Halvorsen K, Thorstensson A. Patellar tendon load in different types of
37 Moseley GL, Arntz A. The context of a noxious stimulus affects the pain it evokes. eccentric squats. Clin Biomech (Bristol, Avon) 2007;22:704–11.
Pain 2007;133:64–71. 60 Frohm A, Saartok T, Halvorsen K, et al. Eccentric treatment for patellar
38 Hodges PW, Moseley GL. Pain and motor control of the lumbopelvic region: effect tendinopathy: a prospective randomised short-term pilot study of two rehabilitation
and possible mechanisms. J Electromyogr Kinesiol 2003;13:361–70. protocols. Br J Sports Med 2007;41:e7.
39 Mokone GG, Schwellnus MP, Noakes TD, et al. The COL5A1 gene and Achilles 61 Jensen K, Di Fabio RP. Evaluation of eccentric exercise in treatment of patellar
tendon pathology. Scand J Med Sci Sports 2006;16:19–26. tendinitis. Phys Ther 1989;69:211–16.
40 September AV, Nell EM, O’Connell K, et al. A pathway-based approach investigating 62 Jonsson P, Alfredson H, Sunding K, et al. New regimen for eccentric calf-muscle
the genes encoding interleukin-1β, interleukin-6 and the interleukin-1 receptor training in patients with chronic insertional Achilles tendinopathy: results of a pilot
antagonist provides new insight into the genetic susceptibility of Achilles study. Br J Sports Med 2008;42:746–9.
tendinopathy. Br J Sports Med 2011;45:1040–7. 63 Kongsgaard M, Aagaard P, Roikjaer S, et al. Decline eccentric squats increases
41 Jewson JL, Lambert GW, Storr M, et al. The sympathetic nervous system and patellar tendon loading compared to standard eccentric squats. Clin Biomech
tendinopathy: a systematic review. Sports Med 2015;45:727–43. (Bristol, Avon) 2006;21:748–54.
42 Butefisch CM, Wessling M, Netz J, et al. Relationship between interhemispheric 64 Mafi N, Lorentzon R, Alfredson H. Superior short-term results with eccentric calf
inhibition and motor cortex excitability in subacute stroke patients. Neurorehabil muscle training compared to concentric training in a randomized prospective
Neural Repair 2008;22:4–21. multicenter study on patients with chronic Achilles tendinosis. Knee Surg Sports
43 Lund JP, Donga R, Widmer CG, et al. The pain-adaptation model: a discussion of Traumatol Arthrosc 2001;9:42–7.
the relationship between chronic musculoskeletal pain and motor activity. Can J 65 Kongsgaard M, Kovanen V, Aagaard P, et al. Corticosteroid injections, eccentric
Physiol Pharmacol 1991;69:683–94. decline squat training and heavy slow resistance training in patellar tendinopathy.
44 Graven-Nielsen T, Svensson P, Arendt-Nielsen L. Effects of experimental muscle pain Scand J Med Sci Sports 2009;19:790–802.
on muscle activity and co-ordination during static and dynamic motor function. 66 Paavola M, Kannus P, Paakkala T, et al. Long-term prognosis of patients with
Electroencephalogr Clin Neurophysiol 1997;105:156–64. Achilles tendinopathy. An observational 8-year follow-up study. Am J Sports Med
45 Le Pera D, Graven-Nielsen T, Valeriani M, et al. Inhibition of motor system excitability at 2000;28:634–42.
cortical and spinal level by tonic muscle pain. Clin Neurophysiol 2001;112:1633–41. 67 Kidgell DJ, Stokes MA, Pearce AJ. Strength training of one limb increases
46 Farina S, Valeriani M, Rosso T, et al. Transient inhibition of the human motor cortex corticomotor excitability projecting to the contralateral homologous limb. Motor
by capsaicin-induced pain. A study with transcranial magnetic stimulation. Neurosci Control 2011;15:247–66.
Lett 2001;314:97–101. 68 Latella C, Kidgell DJ, Pearce AJ. Reduction in corticospinal inhibition in the trained
47 Ngomo S, Mercier C, Bouyer LJ, et al. Alterations in central motor representation and untrained limb following unilateral leg strength training. Eur J Appl Physiol
increase over time in individuals with rotator cuff tendinopathy. Clin Neurophysiol 2012;112:3097–107.
2015;126:365–71. 69 Pearce AJ, Hendy A, Bowen WA, et al. Corticospinal adaptations and strength
48 Nijs J, Daenen L, Cras P, et al. Nociception affects motor output: a review on sensory- maintenance in the immobilized arm following 3 weeks unilateral strength training.
motor interaction with focus on clinical implications. Clin J Pain 2012;28:175–81. Scand J Med Sci Sports 2013;23:740–8.
Method
Preliminary data contained in this supplementary file were collected using the method described below. Participants were recruited from sub-elite
and elite basketball and volleyball populations and were aged over 18 years and all playing / training three times per week. If they were not able
to participate in games and trainings three times per week for any reason including PT, they were not included because of the potential for activity
to modify the primary motor cortex (M1) and motor control as demonstrated in pilot testing.
While habitual activity has been shown to effect the M1, no study was identified that specifically considered the type of activity and
the influence on the M1 and motor drive. Thirteen physically active, healthy participants were recruited (Table 1.) All participants
completed at least three sessions per week of structured activity and included a mix of elite, sub-elite and recreational athletes.
Athletes nominated their dominant leg for testing and the contralateral corticospinal excitability was tested
Table 1 Characteristics of participants in the pilot study that investigated the influence of jumping on corticospinal excitability
Characteristics Description
N (men) 13 (9)
(median+range)
BMI (mean±SD) 23.87±2.60
Weekly activity Australian football, swimming, touch football, running, martial arts, volleyball
and badminton
Following testing, participants were grouped according to activity type (jumping yes/no). Data were coded and all data were analysed
blinded to group activity type (Table 2). Stimulus response curves were constructed (normalised to MMAX) and the slope was
calculated using GraphPad Prism. Data for MMAX, active motor threshold (AMT) and maximal voluntary isometric contraction
(MVIC) are presented as median and range. In order to be conservative, non-parametric analyses (Mann Whitney U) were conducted
on all comparisons, as the sample size was small and groups were an uneven number. Physically active people who did not participate
in sports that have a jumping requirement exhibited lower corticospinal excitability, evidenced by a decrease in the slope of the
stimulus response curve (higher number indicates decrease in slope) (Table 2).
Table 2 Corticospinal responses, peripheral measures and descriptions of each group
Group by activity (jumping yes Characteristics MMAX AMT MVIC Slope (AU)
/ no)
Martial arts
Volleyball
Badminton
Touch football
Running
AMT, active motor threshold; MVIC, Maximum voluntary isometric contraction; AU, arbitrary units * denotes p=0.002
These data suggest that jumping has a profound effect on the CSE and that it is therefore important that any comparisons made
between controls, those with other AKP or PT participate in jumping sports. Data were checked for the potential effect of gender and
found to be non-significant (p = 0.26). There were no differences between groups for MMAX, AMT or MVIC (p < 0.05).
Based upon these data, the decision was made to recruit both men and women but only include athletes that played / trained at least
Note that the larger randomised clinical trial (RCT) (Rio et al., unpublished data and van Ark et al., unpublished data) included participants aged
over 16 years however, only participants aged over 18 years were offered transcranial magnetic stimulation (TMS) testing.
Athletes were asked to complete a VISA-P, a questionnaire about patellar tendon pain and function that is scored between 0 and 100 with 100
being maximal pain free function [1]. Height in centimetres (cm) using a stadiometer and weight in kilograms (kg) without foot ware were
Patellar tendinopathy (PT) in all studies was diagnosed as localised pain at the inferior pole of the patella during jumping and landing as well as
during the single leg decline squat (SLDS), a reliable patellar tendon pain provocation test [3]. Grey scale ultrasound (US) was used to confirm
the diagnosis by applying the following where at least one criterion had to be satisfied; presence of a hypoechoic area, increased thickness of the
anterior/posterior diameter greater than six millimetres (mm) or the presence of vessels. Athletes with bilateral symptoms were asked to nominate
their most painful knee on the SLDS using a numerical rating scale (NMR) 0-10 and measures of quadriceps torque were taken from this side only
Inter-person data
Jumping athletes were recruited and offered bilateral TMS testing. Following testing, they were assessed clinically and using US to determine the
presence of tendon pain (NRS pain on SLDS) and tendon pathology (US) for sub-grouping into unilateral or bilateral tendon pain or pathology.
In-season intervention study - Tendon neuroplastic training
Concealed randomisation was achieved by asking the athlete to draw an opaque sealed envelope with no external markings [4]. The envelope
contained a number (either one = isometric or two = isotonic) produced by random number generation (Excel 2007©).
Data were collected as part of a RCT with two intervention arms completed over four weeks during a competitive season. The intervention was
completed four times per week. There were two active intervention arms, either isometric or isotonic muscle contractions and no sham group.
maximum (for the isotonic group) and MVIC (for the isometric group) were determined for starting loads. As muscle work during isometric
exercise and isotonic exercise cannot be directly measured, protocols were matched for rating of perceived exertion on the basis of pilot studies
and to avoid delayed onset muscle soreness as this was an in season study and muscle pain may negatively affect compliance or sporting
participation. Furthermore, the protocol were matched for time under tension and based upon data supporting the use of external pacing to
Auditory cues have been shown to be beneficial on the induction of neuroplasticity [6-11]. Therefore both groups received an auditory file to play
on their smart phone device during their exercise sessions that provided verbal instructions and paced the muscle contractions (Table 3). The aims
of this were to try to ensure timing was adhered to, provide auditory stimulation and avoid self-pacing so that the only difference between groups
seconds
External pacing and cues Metronome and verbal Metronome and verbal
instructions instructions
100 degrees
Note: the protocol was modified from [2] to prevent delayed onset muscle soreness.
Single pulse TMS was used to obtain stimulus response curves and paired pulse TMS technique was used to quantify SICI and these methods have
For the inter-person study, outcome measures were active motor threshold, CSE and SICI. For the RCT, outcome measures were short interval
cortical inhibition (SICI) and VISA-P. Non-parametric tests were chosen due to small sample size.
Bilateral data was obtained for 16 athletes (32 hemispheres). Of these, four were control participants recruited to compare SICI against the
published physiological normal range for the quadriceps (50-70%) [6, 12] as it was unknown if SICI may be altered in jumping athletes. The
median SICI ratio for both sides of control athletes was 56.81 (range 50.86-58.81) and there were no differences between hemispheres in control
participants (p=0.49). There were no differences between sides in control participants for the slope of the stimulus response curve, left = 7.28, n=4,
right = 9.55, n=4, p=0.83. This supported data obtained in previous studies of control participants (Rio et al., 2015 accepted) and previously
published physiological ranges [12]. Two athletes for whom bilateral data was obtained were excluded (one swimmer and one rock climber).
This was because significant differences were found in corticospinal excitability of athletes that regularly jumped and those that did not despite the
same number of structured physical activity sessions in a week, in a pilot study of 13 athletes (p=0.002). Therefore, fourteen athletes were
included in the data provided in the paper, n=4 controls and n=10 with tendinopathy.
Nine athletes (seven men and two women) with either unilateral (n=5) or bilateral (n=4) PT who were taking no medication were included in the
study (Table 2). This was part of a larger trial of 29 people, who were all offered inclusion in the TMS component. Nine athletes completed the
study, four in the isotonic group and five in the isometric group.
Baseline
intervention LOT sx height weight BMI KTW L KTW R VISA Leg SLDS MVC AMT M wave curve V50 SICI
M isotonic 84 181.5 74 22.464 11 7 69 R 8 202 26 26.519 0.1004 1.701 41.87
M isometric 24 185 81 23.667 13 8 13 R 7 113 28 18.64 0.2165 1.454 33.82
F isometric 1 178 65.3 20.61 12 11 65.5 R 5 177 33 15.482 0.2368 1.68 56.3
F isotonic 24 170.5 100.9 34.709 12 9 46 L 7 220 29 18.381 0.1493 1.475 24.65
M isometric 36 188 81.1 22.946 12 11 76 R 7 165 36 22.354 0.1283 1.414 41.12
M isotonic 4 183 79.7 23.799 17 16 65 L 5 263 25 17.474 0.1242 1.389 79.74
M isometric 36 182.6 84.1 25.223 7 8 63 L 7 152 35 24.29 0.1239 1.452 28.61
M isotonic 120 194 96.5 25.64 17 17 65 R 9 221 38 22.824 0.1237 1.443 20.17
GROUP 30 182.8 81.05 23.733 12 10 65 7 189.5 31 18.64 0.1283 1.454 41.12
M, male. F, female. LOT sx, length of time of symptoms (months). BMI, body mass index. KTW, knee to wall (cm). SLDS, single leg decline
squat. MVC, maximal voluntary isometric contraction. AMT, active motor threshold. Mwave, maximal compound wave. SICI, short interval
cortical inhibition
The individual data is provided (Table 3,4) including calculated change scores for the outcome measures – VISA-P, SLDS, SICI. Median and
mean are provided, though non-parametric tests were chosen due to small sample size.
inhibition
% MVC
VISA SLDS MVC change AMT M wave curve V50 SICI
Isotonic -2 5 66 32.67327 -3 -1.12718 -0.04745 0.09 49.49833
13 3 8 3.636364 -2 3.604896 0.0843 0.265 46.61606
19 4 67.82 25.78707 0 1.56073 -0.0118 0.056 -4.32399
8 6 59 26.69683 -8 1.904929 -0.05103 0.089 62.81073
Median 10.5 4.5 62.5 26.24195 -2.5 1.732829 -0.02963 0.0895 46.61606
Isometric 28 3 52 46.0177 -2 2.142729 0.0143 2.029 65.6265
32 3 11 6.214689 0 1.18803 0.0982 0.254 25.25372
8 3 64 38.78788 -3 -2.36908 0.0253 -0.007 30.9979
9 5 28 13.7931 -2.5 1.665379 0.0198 1.1415 56.12128
15 4 30 16.66667 0 -0.16 0.074 0.245 23.84107
Median 18.5 3 40 26.29049 -2.25 1.426704 0.02255 0.69775 43.55959
The individual SICI data following the RCT is provided (Table AA5).
1
2 56.30 81.56 25.25
3
41.12 72.12 31.00
4
median
1
24.65 71.2662 46.61606
2
4
20.17 82.97635 62.81073
Group
33.26 77.98 46.62#
median
^ p=0.06, # p=0.25
1. Visentini, P.J., et al., The VISA score: an index of severity of symptoms in patients with jumper's knee (patellar tendinosis). Victorian
Institute of Sport Tendon Study Group. Journal of science and medicine in sport / Sports Medicine Australia, 1998. 1(1): p. 22-8.
2. Rio, E., et al., Isometric exercise induces analgesia and reduces inhibition in patellar tendinopathy. Br J Sports Med, 2015.
3. Purdam, C., et al., Discriminative ability of functional loading tests for adolescent jumper's knee. Physical Therapy in Sport, 2003. 4(1): p.
3-9.
4. Schulz, K.F. and D.A. Grimes, Allocation concealment in randomised trials: defending against deciphering. Lancet, 2002. 359(9306): p.
614-8.
5. Ahtiainen, J.P., et al., Muscle hypertrophy, hormonal adaptations and strength development during strength training in strength-trained
and untrained men. Eur J Appl Physiol, 2003. 89(6): p. 555-63.
6. Goodwill, A.M., A.J. Pearce, and D.J. Kidgell, Corticomotor plasticity following unilateral strength training. Muscle Nerve, 2012. 46(3): p.
384-93.
7. Hendy, A.M., M. Spittle, and D.J. Kidgell, Cross education and immobilisation: mechanisms and implications for injury rehabilitation. J Sci
Med Sport, 2012. 15(2): p. 94-101.
8. Kidgell, D.J. and A.J. Pearce, Corticospinal properties following short-term strength training of an intrinsic hand muscle. Hum Mov Sci,
2010. 29(5): p. 631-41.
9. Kidgell, D.J., M.A. Stokes, and A.J. Pearce, Strength training of one limb increases corticomotor excitability projecting to the contralateral
homologous limb. Motor Control, 2011. 15(2): p. 247-66.
10. Latella, C., D.J. Kidgell, and A.J. Pearce, Reduction in corticospinal inhibition in the trained and untrained limb following unilateral leg
strength training. Eur J Appl Physiol, 2012. 112(8): p. 3097-107.
11. Weier, A.T., A.J. Pearce, and D.J. Kidgell, Strength training reduces intracortical inhibition. Acta Physiol (Oxf), 2012. 206(2): p. 109-19.
12. Weier, A.T., A.J. Pearce, and D.J. Kidgell, Strength training reduces intracortical inhibition. Acta physiologica, 2012. 206(2): p. 109-19.