The nonrigidity of tendon has a profound influence on the performance capability of the human locomotor system during sport and daily activities. The main functions of the tendon during locomotion are: (a) to transfer muscle forces to the skeleton, (b) to store mechanical energy coming from the human body and from muscular work as strain energy, and (c) to create favorable conditions for the muscle fibers to produce force as a result of the force-length-velocity relations. Recent experimental studies on humans report a significant influence of the mechanical properties of tendons on running economy (6), sprint performance (24), and the dynamic stability control after sudden postural perturbations (14).
Earlier in vitro studies demonstrated that long-lasting static and cyclic mechanical loading can have acute effects on the mechanical properties of tendon (1) and contribute to tendon damage (27). Indicators of tendon damage after static or cycling loading are a decrease in the elastic modulus and stiffness of the tendon and an increase in the cyclic energy dissipation (27,29). Thus, changes in the mechanical properties of the tendon during actions such as running or cycling might influence the safety factor (i.e., ratio of tendon ultimate strain to functional strain) of the tendon and its susceptibility to injury. On the other hand, previous studies that have examined the mechanical properties of fibrous connective tissues such as tendons and ligaments have demonstrated their plasticity in response to chronic external mechanical loads (28,30). These studies reported that exercise increased the elastic modulus and ultimate tensile strength and hypertrophied the tendons, whereas immobilization reduced these properties. Knowledge of tendon plasticity in response to short- and long-term mechanical loading in vivo, therefore, may help to improve tendon adaptation, reduce the risk of injury, and augment the performance potential of humans.
The aims of this review were (a) to determine the in vivo effects of the static and cyclic loads associated with submaximal and maximal fatiguing contractions on the mechanical properties of the tendon-aponeurosis and (b) to assess the adaptations experienced by tendons in vivo in response to cyclic strains.
METHODS AND RESULTS
The mechanical properties (strain force relation and elastic modulus) of the triceps surae and quadriceps femoris tendon and aponeurosis have been examined by measuring joint moments, tendon-aponeurosis elongation, and cross-sectional area (CSA) of the tendon using a torque dynamometer (Biodex-System 3, Biodex Medical Systems, Inc), a 7.5-MHz linear array ultrasound probe (Aloka SSD 4000), and a 1.5 T magnet resonance tomography scanner (Magnetom Symphony, Siemens, Germany).
Measurement of the Ankle and Knee Joint Moments
Torque dynamometers typically measure the moment about one axis in three-dimensional space. Investigators typically assume that the moments about the two other axes are negligible. In a two-dimensional calculation, the moment measured by a dynamometer and the resultant joint moment can be influenced by (a) the gravitational forces, (b) the inertial forces, and (c) the compliance of the dynamometer-body system. Most studies of isometric or isokinetic contractions account for the influence of gravitational forces on the measured results. However, the calculated resultant moment is only accurate if the axis of rotation of the dynamometer is identical to the axis of the studied joint. The compliance of the dynamometer arm-leg system causes changes in the lever arm of the reaction force at the ankle/knee joint over the range of motion (3,5). Despite a good initial agreement between the ankle/knee joint axes and the axis of rotation of the dynamometer, a clear shift between both axes is observed during the contraction. Consequently, the moment measured at the dynamometer differs from the resultant moment around the ankle and knee joints. Differences between actual and measured resultant muscle torques ranging from 0.21% to 23% have been reported during maximal isometric plantarflexion contractions (5) and ranging from 0.20% to 17% during maximal isometric knee extension contractions (3). These differences complicated the assessment of the moment-elongation relations of tendons and aponeurosis.
To consider the misalignment of the joint axis and the axis of the dynamometer in our experiments, we calculated the resultant ankle and knee joint moments through inverse dynamics (3,5). Kinematic data were recorded using a Vicon 624 system (Vicon Motion Systems, Oxford, United Kingdom) with eight cameras operating at 120 Hz. To calculate the lever arm of the ankle joint during ankle plantarflexion contraction, the center of pressure under the foot was determined by means of a flexible pressure distribution insole (Pedar, Novel GmbH, Munich, Germany) that was sampled at 99 Hz. The influence of the gravitational forces on the moments was compensated for all subjects before each ankle plantarflexion or knee extension contraction. The moments arising from antagonistic coactivation during the ankle plantarflexion and knee extension efforts were quantified by assuming a linear relation between the amplitude of the surface electromyogram (EMG) of the ankle dorsiflexor or knee flexor muscles and the moment. The relation was established by measuring EMG and moment during one relaxed condition and two submaximal ankle dorsiflexion or knee flexion contractions at each joint angle (17). In the following text, knee and ankle joint moments refer to the joint moment values after correcting for the gravitational forces, the effect of the joint axis alignment relative to the dynamometer axis, and coactivation of the antagonistic muscles.
Measurement of Tendinous Tissue Elongation
The development of the ultrasound technique has enabled the investigation of the mechanical properties of tendon and aponeurosis in vivo. The experimental procedure includes an isometric maximal voluntary contraction (MVC) on a dynamometer and the concurrent measurement of the displacement of a point at the distal aponeurosis of a muscle-tendon unit. The displacement of the analyzed point at the aponeurosis during an MVC, in relation to a skin marker, corresponds to the elongation of the structures distal to the point caused by the exerted tendon force (Fig. 1).
It is very difficult to completely avoid any joint motion using external strap fixations during maximal ankle plantarflexion or knee extension contractions (3,5). The ankle or knee joint rotation during the MVC affects the length of the analyzed muscle-tendon unit and leads to a significant overestimation of the measured elongation of the tendon and aponeurosis (∼58% during maximal ankle plantarflexion contractions) (9). We used a 7.5-MHz linear array ultrasound probe (Aloka SSD 4000) to visualize the distal tendon and aponeurosis of the gastrocnemius medialis and vastus lateralis muscle-tendon units. The ultrasound probe was placed above each muscle belly at about 50% of its length. To correct for the influence of joint rotation on the actual elongation of the tendon and aponeurosis, the additional displacement of the analyzed points has been calculated relative to a fixed skin marker during a passive (inactive muscle condition) motion of the ankle and knee joints (4,23). The tendon force was calculated by dividing the ankle or knee joint moment by the corresponding tendon moment arm, which was based on the data reported by Maganaris et al. (21), and Herzog and Read (12).
Measurement of the CSA of the Achilles Tendon
To determine the CSA of the Achilles tendon along its length, transverse and sagittal T1-weighted magnet resonance images (Fig. 2) were recorded using a 1.5 T scanner (Magnetom Symphony, Siemens AG, Erlangen, Germany) with an image frequency of 64 MHz. Throughout the scan process, the subjects rested in a supine position, and no muscle activity was apparent during the measurements. The transverse images were referenced to two landmarks: the most proximal aspect of the tuberositas calcanei and the most distal aspect of the soleus muscle, the locations of which were identified in sagittal images. The CSA of the Achilles tendon was identified and analyzed at every 10% of tendon length. The elastic modulus of the Achilles tendon was calculated from the relation between tendon stress and tendon-aponeurosis strain from 50% to 100% of the maximum tendon stress by means of linear regression. To calculate the tendon stress (tendon force/tendon CSA), we used the average value of the CSA of the Achilles tendon from 10% to 100% of the tendon length.
Tendon Plasticity to Short-Term Mechanical Loading In Vivo
Tendon exhibits viscoelastic and plastic behavior in response to long-lasting mechanical loading (1). In vitro studies have shown that damage can accumulate in a tendon after long-lasting static and cyclic mechanical loading (27,29). Initial strain, defined as the strain at which the target stress was first reached, seems to be the primary mechanical parameter responsible for the tendon damage that occurs during both static and cyclic loading (29). Although numerous in vitro studies have demonstrated the acute effects of long-lasting static and cycling mechanical loading on tendon compliance, there is little information about the in vivo effects of long-lasting submaximal and maximal mechanical loading on the compliance of tendon and aponeurosis.
In a series of experiments (18-20,26), we examined the strain-force relation of the medial gastrocnemius and vastus lateralis tendon and aponeurosis of younger and older adults before and after three fatiguing protocols: (a) a sustained submaximal isometric contraction (25% and 40% isometric MVC for the knee extensors and ankle plantarflexors, respectively); (b) submaximal concentric isokinetic contractions until task failure (50% and 70% isokinetic MVC for the knee extensors and ankle plantarflexors, respectively); and (c) maximal concentric isokinetic contractions until task failure. Fourteen elderly (65.2 ± 3.6 yr, 175.7 ± 5.4 cm, 76.2 ± 8.8 kg), 12 young (30.4 ± 7.1 yr, 178.6 ± 6.3 cm, 78.7 ± 6.3 kg), and 12 young cyclists (25.1 ± 3.3 yr, 179.9 ± 6.4 cm, 72.3 ± 4.7 kg) participated in these studies. We examined younger and older adults because recent in vivo studies found that the tendon and aponeurosis of older adults are more compliant than those of younger adults (15,13). The higher compliance of an older tendon could lead to greater initial tendon strain at a given force, resulting to an age-related effect of long-lasting loading on tendon compliance. Furthermore, the reported decrease in the glycosaminoglycan concentration in older tendons (11) can influence the mechanisms that transmit tensile forces from fibril to fibril along the interfibrillar matrix, affecting the mechanical behavior of the tendon (22). A lower proteoglycan concentration, changes in its composition, and a decrease in glycosaminoglycan content in older tendons could induce an age-related effect of static or cyclic mechanical loading on the tendon mechanical properties, resulting in a reduced resistance to creep in tendons of older adults. Static loading and cyclic loading were compared because it has been reported that these induce different creep responses in collagenous tissues (ligament) (25).
Tendon Plasticity to Short-Term Mechanical Loading In Vivo
The older adults displayed significantly lower maximal ankle plantarflexion and knee extension moments, but greater strain values at any given calculated tendon force than the younger participants (Figs. 3 and 4). These results indicate that older adults have a more compliant triceps surae and quadriceps femoris tendon and aponeurosis than younger adults, consistent with previous in vivo studies. However, no significant change in the strain-force relations could be identified in either group, neither after the static nor after the cyclic mechanical loading in all testing protocols (Figs. 3-5). Although the younger adults performed the fatiguing contractions at a significantly greater absolute load (greater force level), their initial strain values were similar to those of the older adults (Table). Given the influence of initial strain on the damage caused by loading (29), the similar initial strain might be one possible explanation for the lack of age-related differences in the behavior of the tendon mechanical properties after long-lasting mechanical loading in vivo.
The similarity of the strain-force relation of the tendon and aponeurosis of medial gastrocnemius and vastus lateralis for both age groups after the static loading might be explained by the low values of the tendon and aponeurosis initial strain during these fatiguing protocols (1.9%-3.7%). The elongation of the tendon at these low strain levels arises mainly from straightening the crimp of the collagen fibers. The elastic structural units, such as elastin and microfibrillar proteins, contribute to recovering the crimp of the collagen fibers after stretching and removal of "residual" strain (1). Furthermore, Wren et al. (29) found that in vitro tendon failure took place after 1080 min of static loading at initial strain values of the tendon at approximately 6%. In the present study, both the initial strain and the duration of the fatiguing task were much less (∼7 min for the older adults and ∼4 min for the younger adults).
The strain experienced by the vastus lateralis tendon and aponeurosis during the isokinetic (cyclic) fatiguing contractions was approximately 4.8% during the submaximal (Table) and 5.5% to 6.2% during the maximal fatiguing protocol. Thus, tendon strain did not remain at the toe region of the stress-strain relation, but proceeded into the quasi-linear region, which occurs after the completion of recruitment of fibers and involves the stretching of the straightened fibers. Consequently, the strain values cannot explain why the strain-force relation of the vastus lateralis tendon and aponeurosis were not influenced by the isokinetic fatiguing contractions. In the present study, the tendon and aponeurosis of medial gastrocnemius and vastus lateralis were preconditioned with several submaximal ankle plantarflexions and knee extensions/contractions and two to three MVC before the start of the mechanical loading. In vitro studies have reported that preconditioning usually shifts the load-elongation curve to the right, and that afterward, the load-elongation relation of the soft tissues reaches a steady state. The warm-up used in our in vivo experiments should have moved beyond the primary strain stage (in this stage, loading causes a rapid increase in strain amplitude but a decrease in strain rate over time) (25) into the secondary strain stage, where the strain rate reaches a steady state over time.
However, a long-lasting loading can push the tendon past this steady state of the load-elongation curve and into the tertiary strain stage, where loading increases strain rate and provokes tendon failure. Wren et al. (29) found that tendon failure occurred after approximately 2180 cycles at an initial strain level of 4.0% to 5.5%. In our studies, the participants were not able to maintain the knee extensor target force of 50% of the isokinetic MVC, which corresponded to an initial strain of approximately 4.8%, for more than about 470 cycles in the young group and 640 cycles in the old group. Similarly, the participants could only perform approximately 255 cycles with strain values of 5.5% to 6.2% during the maximal contractions. It seems, therefore, that the task was terminated before the tendon experienced any structural changes. Tendons, regardless of age, are capable of resisting sustained and repetitive submaximal muscle contractions without altering their mechanical properties.
Tendon Plasticity to Long-Term Mechanical Loading In Vivo
Numerous in vitro studies have reported that cyclic strain is an important regulator of the fibroblast's metabolic activity and the maintenance of the tendon matrix (10,16). Furthermore, modulation of the mechanical stimuli can influence human fibroblasts and the proliferation, apoptosis, and expression of proteins. For example, loading of tendon causes a down-regulation of catabolic and an up-regulation of anabolic gene expression (16), whereas immobilization promotes catabolic responses (i.e., degeneration of the extracellular matrix) imposed by an up-regulation of matrix metalloproteinases (2). In general, the strain magnitude, strain frequency, strain rate, and strain duration of the tendon can influence the cellular biochemical responses and the resulting adaptation. Cyclic strain of fibrous connective tissues, such as tendons, may activate mechanotransduction pathways within the extracellular matrix that influence the anabolic and catabolic responses of the tissue.
Accordingly, we examined (7) the force strain relation of the triceps surae tendon and aponeurosis of 66 young male adults (26 ± 5 yr, 183 ± 6 cm, 77.6 ± 6.7 kg). Ten of these participants were young adults not active in sports (control group), 28 were endurance runners, and 28 were sprinters. Because ankle joint moments, stride frequencies, and ground contact times differ for walking (normal activity for the control group), submaximal running, and sprinting, we suggest that the strain magnitude, strain frequency, and strain rate of the triceps surae tendon and aponeurosis differed during these activities; sprinting having the highest values followed by submaximal running and finally walking. Therefore, we expected that the mechanical properties of the triceps surae tendon and aponeurosis would differ between the three groups in an intensity-dependent manner. However,we found that only the sprinters showed lower strain values at the triceps surae tendon and aponeurosis at a given tendon force (Fig. 6), indicating a higher normalized stiffness compared with the endurance runners and non-sport-active adults. Thus, the mechanical properties of the triceps surae tendon and aponeurosis do not show a graded response to sport activity in an intensity-dependent manner, but rather remain at a control level over a wide range of applied strains, and the strain amplitude or frequency must exceed a given threshold to trigger additional adaptations.
Although there is little information in the literature about the effects of controlled modulation in cyclic strain magnitudes applied to the tendon on the adaptation of the mechanical and morphological properties of tendon in vivo, several in vitro studies suggest the existence of a threshold in tendon strain magnitude for triggering a homeostatic perturbation (16). Therefore, we examined the effect of two different exercise interventions (14 weeks, 4 times per week) of cyclic strain applied to the Achilles tendon on the adaptation of its mechanical and morphological properties (8). Both interventions were done at the same frequency (3-s loading, 3-s relaxation) and volume (Fig. 7), but at different magnitudes of tendon strain (2.85% ± 0.99% vs 4.55% ± 1.38% strain). Eleven healthy not strength-trained adults (29.5 ± 5.0 yr, 172 ± 5 cm, 64.1 ± 5.0 kg) exercised one leg at a low strain (55% MVC force) and the other leg at a high strain (90% MVC force). We found that the intervention produced a decrease in strain at a given tendon force, an increase in tendon elastic modulus, and a region-specific hypertrophy of the Achilles tendon (Fig. 8) only in the leg exercised at a high strain magnitude.
These findings provide evidence for the existence of a threshold of strain magnitude that must be exceeded to induce an adaptation in the properties of the tendon and aponeurosis. The Achilles tendon on the leg exercised at the high strain magnitude showed a region-specific hypertrophy (i.e., increase the CSA of the Achilles tendon at 60% and 70% of its length). The higher elastic modulus of the Achilles tendon after the intervention, however, cannot be explained solely by these morphological changes. Rather, there was plasticity in the extracellular matrix of the tendon, such as the density of matrix proteins, cell orientation, and proteoglycan content and composition. The results further show that a mechanical load with a low magnitude of strains (2.5%-3.0%) exerted on the Achilles tendon is not a sufficient stimulus to trigger adaptations in the Achilles tendon, which is consistent with the stimulus provided by the mechanical load applied during daily activities.
Our experimental results show that neither static nor cyclic long-lasting mechanical loading that produces strains of 2% to 6% has an acute effect on the in vivo strain-force relation of the tendon and aponeurosis at the lower extremities. Warm-up exercises precondition the tendons and minimize the possibility of an alteration in their mechanical properties. Muscle is unable to sustain the force for a sufficient duration during fatiguing contractions to induce an alteration in tendon properties. Although the mechanical and morphological properties of tendon can adapt to chronic stimulations, the strain magnitude must exceed some threshold. Strains of 2.5% to 3% applied to the Achilles tendon are not sufficient to evoke an adaptation, presumably because these strains do not exceed those experienced during activities of daily living.
1. Abrahams M. Mechanical behaviour of tendon in vitro, a preliminary report. Med. Biol. Eng
2. Amiel D, Woo SL, Harwood FL, Akeson WH. The effect of immobilization on collagen turnover in connective tissue: a biochemical-biomechanical correlation. Acta Orthop. Scand
3. Arampatzis A, Karamanidis K, De Monte G, Stafilidis S, Morey-Klapsing G, Brüggemann G-P. Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin. Biomech
4. Arampatzis A, Stafilidis S, De Monte G, Karamanidis K, Morey-Klapsing G, Brüggemann G-P. Strain and elongation of the human gastrocnemius tendon and aponeurosis during maximal plantarflexion effort. J. Biomech
5. Arampatzis A, Morey-Klapsing G, Karamanidis K, De Monte G, Stafilidis S, Brüggemann G-P. Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J. Biomech
6. Arampatzis A, De Monte G, Karamanidis K, Morey-Klapsing G, Stafilidis S, Brüggemann G-P. Influence of the muscle-tendon unit's mechanical and morphological properties on running economy. J. Exp. Biol
7. Arampatzis A, Karamanidis K, Morey-Klapsing G, De Monte G, Stafilidis S. Mechanical properties of the triceps surae tendon and aponeurosis in relation to intensity of sport activity. J. Biomech
8. Arampatzis A, Karamanidis K, Albracht K. Adaptational responses of the human Achilles tendon by modulation of the applied cyclic strain magnitude
. J. Exp. Biol
9. Arampatzis A, De Monte G, Karamanidis K. Effect of joint rotation correction when measuring elongation of the gastrocnemius medialis tendon and aponeurosis. J. Electromyogr. Kinesiol
10. Arnoczky SP, Tian T, Lavagnino M, Gardner K, Schuler P, Morse P. Activation of stress-activated protein kinases (SAPK) in tendon cells following cyclic strain: the effects of strain frequency, strain magnitude
& cytosolic calcium. J. Orthop. Res
11. Cetta G, Tenni R, Zanaboni G, De Luca G, Ippolito E, De Martino C, Castellani A. Biochemical and morphological modifications in rabbit Achilles tendon during maturation and ageing. Biochem. J
12. Herzog W, Read LJ. Lines of action and moment arms of the major orce-carrying structures crossing the human knee joint. J. Anat
13. Karamanidis K, Arampatzis A. Mechanical and morphological properties of human quadriceps femoris and triceps surae muscle-tendon unit in relation to aging and running. J. Biomech
14. Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J. Electromyogr. Kinesiol
. doi:10.1016/j.jelekin.2007.04.003, in press.
15. Kubo K, Kanehisa H, Miyatani H, Tachi M, Fukunaga T. Effect of low-load resistance training on the tendon properties in middle-aged and elderly women. Acta Physiol. Scand
16. Lavagnino M, Arnoczky SP. In vitro
alterations in cytoskeletal tensional homeostasis control gene expression in tendon cells. J. Orthop. Res
17. Mademli L, Arampatzis A, Morey-Klapsing G, Brügemann G-P. Effect of ankle joint position and electrode placement on the estimation of the antagonistic moment during maximal plantarflexion. J. Electromyogr. Kinesiol
18. Mademli L, Arampatzis A, Walsh M. Effect of muscle fatigue on the compliance of the gastrocnemius medialis tendon and aponeurosis. J. Biomech
19. Mademli L, Arampatzis A, Walsh M. Age-related effect of static and cyclic loading on the strain-force curve of the vastus lateralis tendon and aponeurosis. J. Biomech. Eng
20. Mademli L, Arampatzis A. Mechanical and morphological properties of the triceps surae muscle-tendon unit in old and young adults and their interaction with a submaximal fatiguing contraction. J. Electromyogr. Kinesiol
21. Maganaris CN, Baltzopoulos V, Sargeant A. Changes in Achilles tendon moment arm from rest to maximum isometric plantar flexion: in vivo
observations in man. J. Physiol
22. Raspanti M, Congiu T, Guizzardi S. Structural aspects of the extracellular matrix of the tendon: an atomic force and scanning electron microscopy study. Arch. Histol. Cytol
23. Stafilidis S, Karamanidis K, Morey-Klapsing G, De Monte G, Brüggemann G-P, Arampatzis A. Strain and elongation of the vastus lateralis aponeurosis and tendon in vivo during maximal isometric contraction. Eur. J. Appl. Physiol
24. Stafilidis S, Arampatzis A. Muscle-tendon unit mechanical and morphological properties and sprint performance. J. Sports Sci
25. Thornton GM, Schwab TD, Oxland TR. Cyclic loading causes faster rupture and strain rate than static loading in medial collateral ligament at high stress. Clin. Biomech
26. Ullrich AC, Mademli L, Arampatzis A. Effects of submaximal and maximal long-lasting contractions on the compliance of vastus lateralis tendon and aponeurosis in vivo. J. Electromyogr. Kinesiol
. doi:10.1016/j.jelekin.2007.10.008, in press.
27. Wang XT, Ker RF. Creep rupture of wallaby tail tendons. J. Exp. Biol
28. Woo SL-Y, Ritter MA, Amiel D, et al
. The biomechanical and biochemical properties of swine tendons - long term effects of exercise on the digital extensors. Connect. Tissue Res
29. Wren TA, Lindsey DP, Beaupre GS, Carter DR. Effects of creep and cyclic loading on the mechanical properties and failure of human Achilles tendons. Ann. Biomed. Eng
30. Yamamoto E, Hayashi K, Yamamoto N. Mechanical properties of collagen fascicles from stress-shielded patellar tendons in the rabbit. Clin. Biomech