Many athletes participating in sports with plyometric loads have experienced pain in their tendons. This pain may be indicative of tendinopathy. For example, many volleyball players have experienced patella tendinopathy and many runners have experienced Achilles tendinopathy. An imbalance in muscle and tendon properties is a possible cause for this injury. In this blogpost, I will explain why this imbalance is a possible cause and how tendons can be effectively trained to reduce this imbalance.
Tendons transmit the forces from muscles to bones and proper cooperation between the muscles and tendons is important for optimal performance and the prevention of injuries. When a muscle contracts, the tendon will be stretched after all slack is removed . If a strong muscle pulls a relatively weak (compliant) tendon, this tendon will stretch (strain) a lot (Figure 1). This strain can lead to micro-injuries in the extracellular matrix due to collagen deformations and tears in tendon fibrils. When this is repeated many times without sufficient recovery, this can ultimately lead to (macro) injuries such as tendinopathy [2, 3]. When a muscle becomes stronger, a tendon must therefore also adjust the mechanical properties to prevent excessive strain and associated damage. An increase in the stiffness of the tendon results in less elongation at an equal force and serves as a protective mechanism. Stronger muscles therefore also need stiffer tendons.
Figure 1. Upper images: Left: imbalance between muscle and tendon properties. A strong muscle (large cross-sectional area) pulling on a compliant tendon results in a high tendon strain. Right: balance between muscle and tendon properties. Muscle contraction results in lower tendon strain.
Below: Multiphoton microscopy images of rat tendons with repeated stretching. Adapted from Fung et al. . (A) non-fatigued tendons show highly aligned, parallel collagen fibers without matrix disorganization. (B) At low fatigue, the tendon microstructure is characterized by isolated kinked fiber deformations (KD) that extend across several fibers. (C) With moderate fatigue, there is an increase in the density of the damage patterns in the matrix and the widening of the space between fibers (IS). (D) In case of high fatigue, there are serious matrix disorganizations, poor alignment of the fibers and a larger widening of the space between fibers. Areas with low signal intensity suggest fiber thinning (TH) and more severe, matrix discontinuities (DC). Field of view = 400 mm.
Imbalance due to training
Muscle and tendon tissue adapt in response to mechanical loading and are therefore sensitive to mechanical stimuli. The process by which a mechanical stimulus is converted into a biochemical response is called mechanotransduction . This biochemical response ensures that adaptations take place. However, the time-course of adaptation [6-9, 2] and the mechanical stimuli that elicit these adaptations can differ between muscle and tendinous tissue [10-12, 2]. Specifically, recent in vivo experiments on the human Achilles tendon show that tendinous tissue is most effectively trained using high loads that induce high strain magnitudes [13, 14, 11, 15]. These experiments also showed that a moderate loading duration (i.e., 3 second loading and relaxation) resulted in more adaptations than a shorter (i.e., 1 second loading and unloading) or a longer (i.e., 12 seconds) loading duration. These findings suggest that tendon tissue is less responsive to high strain magnitudes applied for short durations (e.g., plyometric exercises ) and is minimal to not responsive to low loads. Training, and in particular large volumes of predominantly plyometric training or low mechanical intensity training such as in rehabilitation may therefore lead to imbalances in muscle and tendon properties and therefore eventually result in injury.
“Large volumes of predominantly plyometric training may lead to imbalances in muscle and tendon properties and therefore eventually result in injury.”
Is there evidence for these imbalances?
In a recent cross-sectional study, Mersmann and colleagues showed that adolescent volleyball players exhibited a greater imbalance in knee extensor muscle strength and patellar tendon properties compared to similar-aged recreationally active individuals . Compared to recreationally active adolescents, adolescent volleyball athletes also exhibited greater fluctuations in knee extensor muscle strength that were not accompanied by a matched adaptive response of the patellar tendon over the course of a one-year period . The authors speculated that this imbalance could contribute to the development of patellar tendon injuries in this population due to a combined effect of (plyometric) training and maturation [17, 7, 8, 2]. Similar imbalances between other muscle-tendon complxes such as the gastrocnemius/soleus and Achilles tendon and bicep femoris long head/semitendinosus and conjoint tendon as a result of training and/or maturation may also explain some of the tendon injuries although further research is required to confirm this.
Although a weaker tendon in relation to a stronger muscle may lead to tendon injuries, a too stiff tendon in relation to a weaker muscle may also lead to injuries. When an external force stretches a stiff tendon (for example, the Achilles tendon during the ground contact of running), this stiff tendon will stretch less and transmit more stretch at a faster velocity to the muscle fibers. This can lead to muscle injuries. Therefore, a balance between muscle and leg properties is important to prevent injuries.
In addition to injuries, a too compliant tendon can also reduce performance because the muscle fibers will experience less resistance and will therefore shorten faster. As a result, the muscle fibers work in a less favorable force-length-velocity relationship, which ultimately results in less force production or more energy use to produce the same force . Conversely, a too stiff tendon can also result in a loss of performance because it can store less elastic energy. Preventing imbalances is therefore beneficial from both an injury prevention and a performance enhancement perspective.
What can we do to prevent these imbalances?
An imbalance in muscle and leg properties can be prevented by regularly performing heavy resistance training. In order to be effective for the tendon, the exercises have to meet several characteristics.
In vivo experiments on the human Achilles tendon show that a strain magnitude of about 5% is optimal to train tendon stiffness [14, 13]. This corresponds well with the findings of a recent in vitro tendon model, where a comparable strain magnitude led to the largest increase in phosphorylation (~ activation) of a protein (ERK1/2) involved in the production of collagen . In both the in vivo and in vitro experiments, less strain led to less adaptations / phosphorylation. To get sufficient strain on the tendon, the muscle has to contract strongly. A weight of >85-90% of the maximum voluntary contraction/one repetition maximum leads to a strong muscle contraction and sufficient strain (~ 5%) on the tendon to provide a strong stimulus for adaptation [15, 2]. A weaker muscle contraction can, in combination with a large range of motion also lead to sufficient strain, but can also lead to more compression, which is a risk factor for tendinopathy . A smaller range of motion with a stronger muscle contraction is therefore preferable.
Duration of the load
With very brief loading durations such as in plyometric training (e.g., ground contact time of ~200 ms), the strain is not very effectively transmitted to the cellular level due to mechanisms such a rotation and sliding of tendon fibers, hereby reducing the stimulus for adaptation. In other words, there is no effective mechanotransduction. In vivo studies show that a contraction duration of about 3 seconds with a rest period of 3 seconds leads to tendon adaptations, suggesting an effective mechanotransduction takes place [13, 14, 11, 15]. These studies also showed that a contraction duration of 12 seconds has no extra beneficial effect. These findings agree well with in vitro research where the phosphorylation of a protein involved in the production of collagen was the highest with a contraction duration of 2 seconds . Shorter (1 second) and longer (10 second) contractions resulted in a lower phosphorylation. These findings suggest that a contraction duration of roughly 3 seconds is optimal for achieving adaptations in (healthy) tendon tissue.
Unfortunately, no in vivo research has been carried out to investigate the optimal rest period between sets or training sessions with tendon training. However, because the in vitro and in vivo experiments agree reasonably well with regards to the optimum intensity and duration of the load, the in vitro experiments can provide some information on the optimum rest period between training sessions. In these experiments, the tendon tissue was re-trained after several periods and after a period of about 6 hours of rest, the protein was again maximally responsive to strain [19, 21]. These findings suggest that at least 6 hours of rest is required between training sessions aimed at the tendon.
Although the contraction type (concentric, eccentric or isometric) is not of primary importance in inducing mechanical adaptations to tendons, it is important to consider some advantages and disadvantages of different training methods [15, 22, 23]. In dynamic (concentric-eccentric) training, the tendon experiences high forces only during a short period of the exercise due to changing moment arms. It is therefore recommended to extend the duration of these movements to about 6 seconds so that the stimulus is long enough for effective mechanotransduction . It is also possible to hold a position in which the forces on the tendon are the highest (for example around the 60 degree knee flexion in a back squat for the patella tendon) for a short duration to stimulate the tendon.
In isometric training, it is recommended to train around the optimum length because this is where most force can be produced, resulting in high forces on the tendon. The advantage of isometric training is that the duration and intensity can be controlled more easily compared with dynamic exercises. Exercises can also more easily be modified to avoid compression on the tendon as this is a risk factor for tendinopathy . For example, training the Achilles tendon around a neutral ankle position and training the proximal hamstrings tendon with a neutral hip and nearly fully extended knee in the Roman chair can result in high mechanical loads but avoid excessive tendon compression. Furthermore, there are indications that isometric contractions have a stronger pain-reducing effect than dynamic contractions [24, 25], although this is not confirmed by all studies . When performing isometric exercises, it is recommended to apply this training 3 times a week with about 2 minutes of rest between the sets using the protocol shown in Figure 2.
Figure 2. Evidence-based tendon training protocol adopted from Bohm et al. .
Comparison with existing protocols
Calf raises are often given as a treatment for Achilles tendon tendinopathy. Although these exercises are usually reasonably effective in treating and preventing tendinopathy, the mechanical load is often low (<85-90% 1RM), in particular for well-trained individuals. It has been suggested that protocols with a low mechanical load such as calf raises can lead to a greater imbalance in muscle and tendon properties because the low mechanical stress has more effect on the muscle than the tendon . These protocols are therefore not optimal for training the tendon and might need to be replaced with protocols that ensure a heavier mechanical load on the tendon. A recent systematic review also found that heavy strength training has potential advantages over pure eccentric training for Achilles tendinopathy, although the magnitude of the effect is very small .
Recently, several studies have used a relatively long contraction duration in the treatment of tendinopathy [28, 25, 26, 29, 30]. For example, Rio et al.  found that 5 x 45 sec isometric contractions at 80% of the maximum voluntary isometric contraction lead to acute pain relief and also reduced pain in the long term in individuals with patellar tendinopathy. Another study found pain relief in individuals with patellar tendinopathy with a similar isometric or dynamic protocol, but the pain reduction did not correspond to a change in the tendon structure . However, recent research found no acute pain relief with a similar isometric protocol in individuals with Achilles tendinopathy .
The contraction duration used in these studies is longer than optimal on the basis of the studies discussed above, and therefore it can be questioned whether these protocols are optimal. However, the previously discussed in vivo studies have been performed on tendons of people without tendinopathy and the in vitro study has been performed on a ‘healthy’ piece of tendon tissue. In tendinopathy there can however be tissue damage [31, 32], although not all studies find this . When a damaged tendon is loaded, the strong and intact tendon tissue protects the less strong and damaged tissue. This effect is also called ‘stress shielding’. When the tendon is loaded, the healthy tissue will be loaded mostly and the damaged tissue will therefore not be optimally stimulated to adapt. In order to load the damaged tissue, we can use the stress-relaxation effect. Stress relaxation is a property of viscoelastic materials such as tendons and refers to a decreased tension over time with an equal strain, due to mechanisms such as water displacement and fiber sliding [28, 34]. Because the undamaged collagen fibers slowly relax, the damaged tissue becomes more loaded and thus stimulated to adapt. A large part of this effect is achieved within 30 seconds . Longer contractions may therefore be necessary for tendinopathy to also load and stimulate damaged tissue to adapt. In contrast to the suggestions, changes in the tendon structure were not found after 4 weeks of training with these longer contractions despite improvements in pain . Although this may indicate that the structural changes take place on a scale that is smaller than the resolution of current ultrasound techniques, it may also indicate that these protocols are not very effective to stimulate (especially the damaged) tendon tissue to adapt.
In addition to a change in the mechanical properties of the tendon, stress can cause changes in pain and control from the central nervous system . These adaptations may be better trained with a protocol in which there is a longer contract duration. However, research in which this hypothesis has been investigated is still lacking. Irrespective of the underlying mechanism, it seems wise to (also) use longer contractions in individuals with tendinopathy, especially because changes in tendon structure (and mechanical properties) are not always correlated with pain [36, 30].
Recently it has been shown that taking 15 g of gelatin in combination with ~ 225 mg of vitamin C (from about 30 ml of orange juice) an hour before a training protocol leads to an increase in collagen synthesis compared to the intake of a placebo supplement [28, 37]. This supplement may therefore be used for injury prevention or during rehabilitation  in combination with the previously described exercise protocols. A recent study with 18 participants has shown that exercise therapy (twice a day 90 repetitions of eccentric calf raises with extended leg and flexed knee) for Achilles tendon tendinopathy yielded better results when combined with 2.5 g of gelatin 30 minutes prior to the exercises (and again later in the day) . It is important to note that the amount of proteins in the gelatin can vary between preparation methods and to get sufficient proteins, a supplements with a standardized dose are therefore preferred . Furthermore, 15 g gelatin results in a larger protein synthesis than 5 g and protein concentration peaks around one hour after intake , suggesting 15 g of gelatin can be most beneficial when taking about 1 hour before exercise.
Imbalances in muscle and tendon strength may lead to injuries, but can potentially be prevented by regularly including heavy resistance exercises.
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