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Tendon neuroplastic training: changing the way we think about tendon rehabilitation: a narrative review

Tendinopathy can be resistant to treatment and often recurs, implying that current treatment approaches are suboptimal. Rehabilitation programmes that have been successful in terms of pain reduction and return to sport outcomes usually include strength training. Muscle activation can induce analgesia, improving self-efficacy associated with reducing one's own pain. Furthermore, strength training is beneficial for tendon matrix structure, muscle properties and limb biomechanics. However, current tendon rehabilitation may not adequately address the corticospinal control of the muscle, which may result in altered control of muscle recruitment and the consequent tendon load, and this may contribute to recalcitrance or symptom recurrence. Outcomes of interest include the effect of strength training on tendon pain, corticospinal excitability and short interval cortical inhibition. The aims of this concept paper are to: (1) review what is known about changes to the primary motor cortex and motor control in tendinopathy, (2) identify the parameters shown to induce neuroplasticity in strength training and (3) align these principles with tendon rehabilitation loading protocols to introduce a combination approach termed as tendon neuroplastic training. Strength training is a powerful modulator of the central nervous system. In particular, corticospinal inputs are essential for motor unit recruitment and activation; however, specific strength training parameters are important for neuroplasticity. Strength training that is externally paced and akin to a skilled movement task has been shown to not only reduce tendon pain, but modulate excitatory and inhibitory control of the muscle and therefore, potentially tendon load. An improved understanding of the methods that maximise the opportunity for neuroplasticity may be an important progression in how we prescribe exercise-based rehabilitation in tendinopathy for pain modulation and potentially restoration of the corticospinal control of the muscle-tendon complex.

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 M MAX , 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 three times per week in jumping sports in all studies.
Note that the larger randomised clinical trial (RCT) ( 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 recorded and this has been described previously [2].

Clinical diagnosis of patellar tendinopathy
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 and the contralateral hemisphere was tested with TMS.

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.
Exercises were completed on a leg extension machine ( Figure 1).

Figure 1. An example of a leg extension machine used for the intervention of quadriceps muscle contractions
Both protocols were matched for time under load and rest between sets (set at two minutes to allow muscle recovery) ( Table 3) [5]. Repetition 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 modulate corticospinal excitability and inhibition.
Auditory cues have been shown to be beneficial on the induction of neuroplasticity [6][7][8][9][10][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 was muscle contraction type.

Transcranial magnetic stimulation
Single pulse TMS was used to obtain stimulus response curves and paired pulse TMS technique was used to quantify SICI and these methods have been published elsewhere [2].

Outcome measures and statistical tests
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.

Results of the inter-person study
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.
Therefore, the question posed was -what is the effect of unilateral pain on the other side (n=8)?

Results from randomised clinical trial -tendon neuroplastic training
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.  The individual SICI data following the RCT is provided (Table AA5).