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Heterogeneous Loading of the Human Achilles Tendon In Vivo

Bojsen-Møller, Jens1; Magnusson, S. Peter2

Exercise and Sport Sciences Reviews: October 2015 - Volume 43 - Issue 4 - p 190–197
doi: 10.1249/JES.0000000000000062
Articles
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The free Achilles tendon is considered a homogeneous structure that transmits muscular force in a linear manner. However, the tendon undergoes longitudinal rotation and is separated in mechanically independent segments with distinct mechanical and material tissue properties. The present article examines the hypothesis that the human Achilles tendon is loaded asymmetrically and undergoes heterogeneous deformation during movement.

The present article examines the hypothesis that the Achilles tendon is loaded asymmetrically and undergoes heterogeneous deformation during human movement.

1Department of Physical Performance, Norwegian School of Sport Sciences, Oslo, Norway; and 2Institute of Sports Medicine Copenhagen & Musculoskeletal Rehabilitation Research Unit, Bispebjerg Hospital, University of Copenhagen, Copenhagen, Denmark

Address for correspondence: Jens Bojsen-Møller, Ph.D., Norwegian School of Sport Sciences, Sognsveien 220 0860, Oslo, Norway (E-mail: jens.bojsen.moller@nih.no).

Accepted for publication: June 2, 2015.

Associate Editor: Roger M. Enoka, Ph.D.

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INTRODUCTION

The Achilles tendon transmits contractile force from the main plantarflexor muscles, the soleus and the medial and lateral gastrocnemii. Force is transmitted from the contractile tissue through an intricate system of aponeuroses onto the Achilles tendon and the calcaneus bone. This entire muscle-tendon unit is termed the triceps surae. The free Achilles tendon (i.e., the tendon distal to the soleus insertion) is one of the largest tendons in the human body, and it is subjected to remarkably large loads during human locomotion, in sports activities and activities of daily life. In fact, loads of up to 11 kN cm−2 or 12 times body weight have been reported during jumping and running (13,23). The tendon contributes significantly to movement economy by storing and releasing energy during loading and unloading and, moreover, the triceps surae muscle-tendon unit enables energy dissipation when required, for example, during high force landings (1,15,21).

The Achilles tendon is a frequent site of injury, and the most common condition is chronic pain (tendinopathy). Moreover, unlike other human tendons, rupture of the Achilles tendon is rather frequent (6,24). Achilles tendon rupture is considered to be related to a low safety factor, which suggests that the tendon operates closer to the yielding or rupture point than most other human tendons during high load activities. This low safety factor is likely the result of the trade-off in design between the ability of the tendon to store and release energy and the stiffness and strength of the structure (21).

Tendons and their serially coupled aponeuroses have been considered traditionally homogeneous structures that convey force from the contracting muscles to bone in a linear manner; however, technological advances have in recent years enabled more detailed investigation of the tendinous tissues and their functional interplay with associated muscles in vivo. Recent studies suggest that the structure and function of the force transmitting tissues in general is more intricate than previously thought. Specifically, the Achilles tendon seems to undergo longitudinal rotation and to consist of mechanically independent subportions. Moreover, regional differences in mechanical and material tendon properties may be present (3,4,7,10,28,34).

The present article examines the hypothesis that the Achilles tendon is loaded asymmetrically and undergoes heterogeneous deformation during human movement. Moreover, the consequence of such behavior for function and dysfunction is discussed.

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ANATOMICAL DESIGN OF THE ACHILLES TENDON

The force-bearing tissues of the triceps surae consist of separate aponeuroses that merge into the free Achilles tendon distal to the insertion of the soleus muscle. The Achilles tendon has been the subject of study for more than a century; when examining a variety of mammal tendons, Parson (32) described a longitudinal torsion or rotation of the Achilles tendons (Fig. 1). Furthermore, Parson (32) noted that portions of the Achilles tendon seemed to be independent and, on “untwisting” of one canine Achilles tendon, the single-tendon subunits became “unseparated” and “lay parallel to one another.”

Figure 1

Figure 1

More recently, it also has been reported in humans that the force-bearing tissues of the Achilles tendon are mechanically separated well into the free tendon such that tissue bundles that originate from each of the three muscle compartments can be distinguished close to the tendon insertion on the calcaneal bone (8,10,34).

Longitudinal Achilles tendon rotation has been reexamined in later studies, and it seems that the fascicles or collagen tissue bundles that originate from each muscle compartment undergoes internal rotation from proximal to distal such that the Achilles tendon of the right leg undergoes counterclockwise rotation (seen from a cranial viewpoint) from proximal to distal, whereas the tendon of the left leg undergoes clockwise rotation (Fig. 2) (8,10,32,34). The degree of rotation is difficult to quantify, and there is large interindividual variation, however, numbers between 10 and 150 degrees have been reported (10). One very recent study examined 110 cadaver legs and found proximal to distal tendon rotation in all. Depending on the degree of rotation, the specimens were classified in three groups. In the least-rotation group, the soleus inserted anteromedially and the gastrocnemii inserted posterolaterally, which occurred in 50% of the tendons. In the moderate rotation group, the soleus inserted medially and the lateral gastrocnemius inserted anterolaterally, and this occurred in 43% of tendons. In the extreme rotation group, the soleus inserted posteromedially and the lateral gastrocnemius inserted anteriorly whereas the medial gastrocnemius inserted posterolaterally, and this occurred in 7% of tendons. There were no differences observed between sexes or between the left side and the right side (10).

Figure 2

Figure 2

Tendon rotation, thus, is present in the triceps surae, but the function of the tendon rotation remains unknown. Some authors have suggested that a rotated tendon acquires ropelike properties (7,32), and one feature of twisted ropes is to enhance the ability to strain and store energy. An alternative explanation was suggested recently in a modeling study on masseter muscles in fish, in which muscle and tendon rotation occurs (9). The study demonstrated that, in broad muscles that operate at a distance from the joint axis of rotation, and where the insertional tendon attaches over a wide area of bone, variation might occur in the muscle fibers’ abilities to exert force simply because of differences in fiber length through the joint range of motion (9). In such muscle-tendon units, suboptimal force production may occur because of a subset of fibers that are operating outside the plateau of the length-tension curve. A rotated tendon, or a design where the muscle fibers rotate or cross each other, was shown to equalize force-length properties for muscle fibers of the broad muscle, thereby optimizing contractile ability. The human triceps surae is in fact a broad muscle that operates at a significant distance from the joint compared with most other dorsi and plantarflexors of the lower leg. Moreover, the Achilles tendon does display a quite broad insertional or enthesis area on the calcaneus as seen in the transverse plane, which again is different from that of most other muscles crossing the ankle joint. Other human muscle-tendon units that display rotation are those of the pectoralis major and the latissimus dorsi, which both are wide muscles with a large region of origin and a somewhat large area of insertion. Nonetheless, it remains unknown if tendon rotation in humans has in fact the consequences for muscle force exertion that are seen in the masseter muscles of the spotted ratfish (9).

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EVIDENCE OF ASYMMETRICAL ACHILLES TENDON LOADING

From a functional perspective, the Achilles tendon is associated with three separately activated muscles that govern the loading of the tendon, and studies suggest that the tendon consists of mechanically separate tendon portions that each relate to the single muscle compartments (8,34). In cadaver preparations, it has been demonstrated that separate loading of the single triceps surae muscles leads to heterogeneous loading of the Achilles tendon (3). More recently, the triceps surae of cadaver preparations was examined and, when the joint angle of the subtalar joint was manipulated, the calcaneal inversion or eversion influenced the strain profile of the Achilles tendon (25). In a human in vivo model, Magnusson et al. (28) examined differences in mechanical properties of the tendon and associated aponeuroses and, to enable identifiable tendon fixed points (by ultrasonography), thin needles were inserted transversely into the Achilles tendon and, hereafter, subjects performed maximal plantarflexor contractions. When the needles were retracted, some were distorted permanently (Fig. 3), which seems to be direct evidence of nonuniform Achilles tendon deformation in vivo.

Figure 3

Figure 3

Additional investigations have been conducted in vivo, and one study examined muscle displacement in the triceps surae muscles during different joint configurations of the leg (7). These results indicated the occurrence of uneven Achilles tendon loading and suggested that knee joint position and, thus, length of the gastrocnemius muscles play a role in tendon loading (Fig. 4) (7). More recently, uneven deformation of the free Achilles tendon was seen with ultrasonography-based speckle tracking, and greater displacement (∼20%) was observed in the deep layer of the tendon compared with superficial aspects during passive dorsiflexion (2) (Fig. 5). A comparable study examined passive and eccentric loading of the free Achilles tendon during different knee joint configurations by use of ultrasound elastography (33). Here, the middle and deep (anterior) portions of the Achilles tendon underwent greater displacement (∼5–9 mm during an ankle joint excursion of 30 degrees) compared with the posterior area of the tendon (∼4–6 mm of displacement) (33) (Fig. 5). An additional study by the same research group examined anteroposterior Achilles tendon displacement during walking, and a similar pattern of uneven tendon deformation was observed where greater displacement was seen in the ventral part of the tendon (12). Together, these studies are examples of techniques such as robot vision tracking and elastography that may be promising tools for assessing biomechanical tendon function. However, it should be kept in mind that substantial interindividual variation exists in Achilles tendon design and/or rotation (8,10,34), which makes it difficult to ascribe the observed displacement of tendon regions to single muscle compartments of the triceps surae. To increase the biomechanical understanding of tendon function, future studies need to determine, on an individual basis, which parts of the tendon are associated with each of the separate muscles and, hereafter, load- and/or contraction-induced tendon deformation can be investigated in greater detail.

Figure 4

Figure 4

Figure 5

Figure 5

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MECHANISMS FOR ASYMMETRICAL LOADING

Given the multifaceted structure of the triceps surae muscle-tendon unit, there are several potential mechanisms for asymmetrical loading and strain of the Achilles tendon:

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Muscle-Tendon Unit Design

The physiological cross-sectional area of the three triceps surae muscles, which is proportional to force-generating capacity, has been examined previously, and the lateral gastrocnemius is by far the smallest muscle with approximately 7% of the total triceps surae physiological cross-sectional area. The medial gastrocnemius represents approximately 20%, and the soleus has approximately 73% of the total physiological cross-sectional area (14). With respect to muscle volume, the soleus is reported to contain approximately 55% of the total triceps surae volume, whereas the medial and lateral gastrocnemii represent approximately 30% and 15%, respectively (14,22). Thus, the three muscle compartments are quite different with respect to maximal force capability, and it also should be kept in mind that because the gastrocnemii are two-joint muscles, knee joint position also will influence their force-generating capacity. Deformation or strain of the tendinous structures during loading relates to tendon stress (load/tendon cross-sectional area), and a greater tendon area will increase stiffness and, thus, reduce strain for a given load. It is possible that the cross-sectional areas of the separate Achilles tendon compartments (that distinctly are associated with each muscle compartment (10)) correspond to the contractile abilities of each muscle compartment (i.e., similar muscle-tendon cross-sectional area ratio between the compartments), which would result in uniform tendon loading and deformation at maximal exertion. But if a difference exists in muscle-tendon area ratio between the three subunits or if muscle compartments are activated unevenly in relative terms (% max), these are potential candidates for heterogeneous Achilles tendon deformation. The ratio between the physiological muscle cross-sectional area of the three single muscles and the associated cross-sectional area of their respective tendon subunit remains to be investigated, and such information will have great relevance for future understanding the Achilles tendon function and loading profile.

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Neural Activation

In addition to anatomical design, neural activation also may influence the load distribution in the Achilles tendon because the three muscles of the triceps surae are activated independently by the nervous system. Plantarflexor activation has been examined during different contractile tasks with surface electromyography, and it seems clear that neural activation differs between muscles depending on contraction type and/or joint configuration (31,35). Recently, the activation of the triceps surae muscles was examined combining electromyography and positron emission tomography. In line with previous work where contractions were performed with an extended knee joint, the muscles seemed to be heterogeneously activated such that the medial gastrocnemius showed higher intensity compared with the soleus and medial gastrocnemius (30). One recent study examined muscle activation and its distribution within the triceps surae by use of T2 magnetic resonance imaging during plantarflexor efforts with the knee joint extended. With this technique, activated intermuscular regions could be visualized elegantly and, interestingly, a greater (relative) volume (∼50%) of the medial gastrocnemius was activated, whereas the relative activated volume of the soleus and the lateral gastrocnemius was approximately 35% (22). Moreover, longitudinal differences were observed in activated muscle volume within the medial gastrocnemius (neuromuscular compartmentalization), which suggests that the nervous system by precise activation can control the exact force output or joint moment carefully to accommodate the contractile task. Taken together, neural activation of the triceps surae muscles is intricate, and it is plausible that joint configuration and uneven activation of the single muscle compartments may induce heterogeneous Achilles tendon deformation.

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Material and Structural Tissue Properties

The stiffness of the structure is not only governed by tendon cross-sectional area but also the material properties of the tissue. Although there may be differences in material properties between tendons of one individual, the force-bearing tissue within one muscle-tendon unit generally has been considered similar with respect to tissue morphology. Nonetheless, differences in material properties have been observed within different regions of the same human tendon. It has been shown that modulus, peak, and yield stress differ in the anterior compared with the posterior portions of the human patellar tendon (16,17). Similar data are until now not available for the human Achilles tendon, but longitudinal variation in strain of the serially coupled aponeurosis and tendon has been observed during loading (11). Furthermore, it has been shown that the stiffness of the aponeurosis (maximal strain <2%) exceeded that of the free tendon in vivo (maximal strain app 8%) (28,29). Difference in strain between tendons and aponeuroses may result from the mechanical effect of contractile tissue that inserts on the aponeurosis (26) and/or to differences in neural activation within the muscle volume such that, during specific tasks, only parts of the muscle is activated, which in turn modulates the loading of the force-bearing tissue (22,35). Moreover, aponeurosis properties may be modulated by loading in the transverse plane that increases stiffness in the perpendicular plane (the longitudinal direction) via mediolateral deformation, according to Poisson ratio. In fact, both animal and human studies have demonstrated such biaxial strain during active loading that in turn influenced mechanical properties in the longitudinal direction (5,20). If the separate aponeuroses change properties in an uneven manner during contraction, this in turn may result in reduced coalescing of the contractile forces and potentially contribute to uneven loading of the more distal tendon. The magnitude of these effects during daily loading and the influence on the function of the muscle-tendon unit remain to be understood, but it seems likely that the in vivo mechanical and material properties may influence functional capacities such as the ability to store and release energy, to transmit force accurately, or to act as a mechanical damper.

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ACHILLES TENDON DESIGN AND HETEROGENEOUS LOADING FUNCTION AND DYSFUNCTION

Why Tendon Rotation?

As mentioned previously, tendon rotation may reflect a design that enables muscle fibers that are situated far apart in the associated muscles to operate at more similar lengths during the full joint range of motion (9), but whether such a mechanism pertains to the Achilles tendon is not yet known. Another hypothesis is that the rotation facilitates the ability to store and release energy during loading and unloading, respectively. Ropes are engineered in different ways such that twisted ropes are designed for situations where high strains and storage of mechanical energy are required, whereas ropes with parallel fibers are used when minimal strain is required. This analogy may seem reasonable for human tendon design because some tendons are more involved in position control and effective force transmission, such as, for example, tendons of the hand or forearm, whereas the Achilles tendon (in addition to the transmission of force) is highly involved in energy storage and release during locomotion. Previous studies have, in fact, argued for the existence of a trade-off between position control and energy storage and release for tendon design (7). Finally, tendon rotation could serve to regulate intratendinous pressure during the extremely high stresses and strains that are imposed particularly on the Achilles tendon. In a coherent or linear structure, internal pressure is reduced more under tensile stress compared with a rotated structure. Albeit highly speculative, modulation of intratendinous pressure may play a role for maintaining vessel and nerve function and potential fluid diffusion that in turn may relate to the health and function of the tissue.

The exact role of Achilles tendon rotation remains unknown but, if future imaging technologies can enable quantification of tendon rotation in vivo, this would be a powerful model to examine the role of rotation on, for example, movement performance and economy of movement and/or injury given the large interindividual variation (10).

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Why Heterogeneous Deformation?

Functionally, the triceps surae muscle-tendon unit mainly is considered to be responsible for plantarflexion but, because the subtalar joint axis passes laterally to the calcaneal insertion of the tendon, the triceps surae also is a strong inverter of the foot. If the three triceps surae muscles are connected functionally to separate tendon compartments, such a design would enable greater control of ankle and subtalar joint moments because each muscle can function as a separate actuator. For example, given the tendon rotation described above, the soleus muscle inserts on the medial side of the Achilles tendon and therefore at a greater distance to the inversion-eversion joint axis. This means that, hypothetically, the soleus can selectively contribute to inversion to a greater extent than the gastrocnemius muscles. Concurrently, the medial gastrocnemius, which by far has the largest cross-sectional area of the gastrocnemius muscles, inserts posteriolaterally in the Achilles tendon, which could be a mechanism to optimize plantarflexion or even eversion moment about the ankle joint. Extending this line of thought, it should be kept in mind that the gastrocnemius muscles are two-joint muscles that span both the ankle (and subtalar) and knee joint. Therefore, knee joint position during, for example, human gait may in fact influence the length and, thus, contractile abilities of the gastrocnemius muscles. For example, during the latter part of the stance phase during running, the ankle joint moves into plantarflexion while the knee joint is extending, which means that mechanical energy may be transferred from knee joint extensors into plantarflexion (15). At the same time, if the medial gastrocnemius transmits force via a separate tendon portion within the Achilles tendon, the knee joint extension may optimize the length of the gastrocnemius muscle with respect to creating a maximal plantarflexion moment. Furthermore, if the two gastrocnemius muscles inserts into the posterolateral part of the Achilles tendon insertion zone, the effect on plantarflexion or even eversion moment that occurs in the final part of the stance phase may be optimized even further simply by anatomical design. It is clear that such mechanisms remain speculative and warrant confirmation.

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Tendon Injury and Rehabilitation

Although one of the strongest tendons in the body, repetitive loading of the Achilles tendon often leads to overuse injuries, including tendinopathy. Tendinopathy is characterized by pain, tenderness on palpation, local swelling, and impaired performance (6,24). Tendinopathy is a considerable problem in both elite and recreational athletes. In fact, in runners, the incidence of tendon injuries has been estimated to be 22%, with a lifetime cumulative incidence as high as 52% (24,27). Moreover, the symptoms and reduction in performance may be quite protracted and last for years. The exact injury mechanism remains elusive, but understanding how tendon tissue is mechanically loaded might be a key to understanding the pathogenesis and, thus, provide the basis for injury prevention. As mentioned previously, it is possible that the free Achilles tendon is subjected to heterogeneous loading because i) the Achilles tendon is coupled to three distinct muscles with separate neural innervation, ii) the three separate muscles include one- and two-joint muscles and are, therefore, influenced by both ankle and knee joint position, and iii) the Achilles tendon insertion is relatively wide and is, therefore, mechanically influenced by subtalar inversion and eversion. Taken together, changes in tendon loading may result from unfavorable neural activation or from a suboptimal position of the subtalar joint. But also acute changes such as fatigue-induced adaptation in neural activation or even locomotion on unusual or slanted surfaces may influence tendon loading. Significant interindividual variation has been observed with respect to Achilles tendon rotation (8,10), but if similar variation exists with respect to the mechanical separation of the Achilles tendon subportions and, furthermore, whether tendon rotation or mechanical heterogeneity is related to injury remain to be examined.

Different treatment strategies have been described in the literature, but loading interventions have become an accepted form of treatment for tendinopathies (6), and the promising outcome may in fact relate to mechanical loading and tissue deformation. To fully engage all three muscles and thus the entire free Achilles tendon, any rehabilitation strategy would need to include exercises with some degree of knee flexion and full knee extension while performing resisted ankle motion throughout the joint range of motion. This approach would engage all the tendon tissues, but also perhaps create some intratendinous shear. It remains to be established if such loading and/or shear is in fact advantageous in a rehabilitation perspective. Tendon fascicles are separate functional units of tendons, and nerves and vessels are located in the intrafascicular space that may “see” the shear (18). As previously mentioned, it has been shown that calcaneus position may yield intratendinous strain differences by up to 15% (Fig. 6), and, therefore, it also may be important to consider rear foot positioning during the resisted plantarflexion exercises (25). It seems that calcaneal eversion yielded a greater strain of the medial portion of the Achilles tendon while the opposite held true for calcaneal inversion and, therefore, changes in footwear to control or modify the range of motion of the subtalar joint during gait also potentially may be implemented in rehabilitation.

Figure 6

Figure 6

As such, loading regimens yield good clinical results, and although especially eccentric loading has received some attention, there remains little support for the advantage of isolated eccentric training (6). Currently available studies rarely used comparable load magnitudes when comparing eccentric training with other loading regimens, but muscles can produce greater maximal force eccentrically than concentrically and this is rarely exploited during rehabilitation exercises. Moreover, animal work shows that concentric or eccentric contraction to the same force level does not differentially influence the expression of collagen at the cellular level and, even if the eccentric contraction force exceeds that of the concentric contraction, the collagen expression remains the same (19). It remains outside the scope of this review but, collectively, these findings demonstrate that cellular and tendon tissue responses seem independent of contraction mode and, thus, question whether contraction mode is of importance during rehabilitation of tendon injury.

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CONCLUSIONS AND PERSPECTIVES

The present article examined the hypothesis that the Achilles tendon is loaded asymmetrically and undergoes heterogeneous deformation during human movement. The Achilles tendon seems to consist of distinct portions each associated with the three muscle compartments and, furthermore, the tendon portions undergo rotation about the longitudinal axis. Heterogeneous tendon deformation may be associated with issues related to anatomical design, by different material or structural properties in the force-bearing tissues, or by uneven neural activation of muscles. The consequence of heterogeneous deformation for tendon performance, function, and injury is not currently known. Future studies should investigate neural activation of the triceps surae muscle compartments in different tasks, enable measurement of tendon rotation in vivo, and determine anatomical design features such as muscle-tendon cross-sectional area ratio of the single muscles. Moreover, specific tendon loading should be examined in a detailed manner during different contractile tasks. Hereby, the role of heterogeneous Achilles tendon loading with respect to tendon function, force transfer, and energy storage and release may be understood in greater detail. The biomechanical role of Achilles tendon function should be examined with the goal of understanding performance in various contractile tasks. Finally, the role of tendon mechanics in dysfunction and injury should be investigated such that mechanisms of injury can be exposed and, thereby, enable development of more optimal rehabilitation and injury prevention strategies.

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Keywords:

Achilles tendon; tendon function; tendon rotation; tendon injury; heterogeneous tendon deformation

© 2015 American College of Sports Medicine