Effect of joint rotation correction when measuring elongation of the gastrocnemius medialis tendon and aponeurosis

It is well known that during maximal plantar flexion contractions the ankle joint rotation overestimates the actual elongation of the tendon and aponeurosis. The aim of this study was to examine the influence of the curve length changes of the Achilles tendon on the joint rotation corrected elongation and strain of the gastrocnemius medialis (GM) tendon and aponeurosis. Nine subjects (age: 29.4 ± 5.7 years, body mass: 78.8 ± 6.8 kg, body height: 178 ± 4 cm) participated in the study. The subjects performed maximal voluntary isometric plantarflexion contractions in the prone position on a Biodex-dynamometer. Ultrasonography (Aloka SSD 4000) was used to visualize the muscle belly of the GM muscle-tendon unit. To calculate the curve length changes of the Achilles tendon its surface contour was reconstructed using a series of small reflective skin markers having a diameter of 2.5 mm. The elongation of the GM tendon and aponeurosis was calculated (a) as the difference of the measured and the passive (due to joint rotation) displacement of the tendon and aponeurosis and (b) as the difference of the measured displacement and the length changes of the reconstructed Achilles tendon surface contour. The absolute difference between the elongation obtained by both methods were 1.2 ± 0.4 mm. These differences were due to the higher changes in length obtained by the reconstruction of the tendon curved surface contour as compared to the changes observed in the passive displacement of the digitised point at the aponeurosis. Without correcting for angle joint rotation, the measured elongation clearly overestimates the actual elongation of the GM tendon and aponeurosis. After the passive displacement correction the calculated elongation still overestimates the actual elongation of the GM tendon and aponeurosis. However, this overestimation has a negligible effect on the examined in vivo strain (0.3%) of the tendon and aponeurosis.     

Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo.

Load-strain characteristics of tendinous tissues (Achilles tendon and aponeurosis) were determined in vivo for human medial gastrocnemius (MG) muscle. Seven male subjects exerted isometric plantar flexion torque while the elongation of tendinous tissues of MG was determined from the tendinous movements by using ultrasonography. The maximal strain of the Achilles tendon and aponeurosis, estimated separately from the elongation data, was 5.1 +/- 1.1 and 5.9 +/- 1.6%, respectively. There was no significant difference in strain between the Achilles tendon and aponeurosis. In addition, no significant difference in strain was observed between the proximal and distal regions of the aponeurosis. The results indicate that tendinous tissues of the MG are homogeneously stretched along their lengths by muscle contraction, which has functional implications for the operation of the human MG muscle-tendon unit in vivo.     

Effect of muscle fatigue on the compliance of the gastrocnemius medialis tendon and aponeurosis

The aim of the present study was to examine whether or not the compliance of the gastrocnemius medialis (GM) tendon and aponeurosis is influenced by submaximal fatiguing efforts. Fourteen elderly male subjects performed isometric maximal voluntary plantarflexion contractions (MVC) on a dynamometer before and after two fatiguing protocols. The protocols consisted of: (1) submaximal concentric isokinetic contractions (70% isokinetic MVC) at 60 degrees /s and (2) a sustained isometric contraction (40% isometric MVC) until failure to hold the defined moment. Ultrasonography was used to determine the elongation and strain of the GM tendon and aponeurosis. To account for the axis misalignment between ankle and dynamometer, the kinematics of the leg were captured at 120 Hz. The maximum moment decreased from 85.9+/-17.9 Nm prior fatigue to 79.2+/-19 Nm after isokinetic fatigue and to 69.9+/-16.4 Nm after isometric fatigue. The maximal strain of the GM tendon and aponeurosis before fatigue, after isokinetic and after isometric fatigue were 4.9+/-1.1%, 4.4+/-1.1% and 4.3+/-1.1% respectively. Neither the strain nor the elongation showed significant differences before and after each fatiguing task at any 100 N step of the calculated tendon force. This implies that the compliance was not altered after either the isokinetic or the isometric fatiguing task. Therefore it was concluded that the strains during the performed submaximal fatiguing tasks, were too small to provoke any structural changes in tendon and aponeurosis.     

Superficial aponeurosis of human gastrocnemius is elongated during contraction: implications for modeling muscle-tendon unit.

Two questions were addressed in this study: (1) how much strain of the superficial aponeurosis of the human medial gastrocnemius muscle (MG) was obtained during voluntary isometric contractions in vivo, (2) whether there existed inhomogeneity of the strain along the superficial aponeurosis. Seven male subjects, whose knees were extended and ankles were flexed at right angle, performed isometric plantar flexion while elongation of superficial aponeurosis of MG was determined from the movements of the intersections made by the superficial aponeurosis and fascicles using ultrasonography. The strain of the superficial aponeurosis at the maximum voluntary contraction, estimated from the elongation and length data, was 5.6+/-1.2%. There was no significant difference in strain between the proximal and distal parts of the superficial aponeurosis. Based on the present result and that of our previous study for the same subjects (J. Appl. Physiol 90 (2001) 1671), a model was formulated for a contracting uni-pennate muscle-tendon unit. This model, which could be applied to isometric contractions at other angles and therefore of wide use, showed that similar strain between superficial and deep aponeuroses of MG contributed to homogeneous fascicle length change within MG during contractions. These findings would contribute to clarifying the functions of the superficial aponeurosis and the effects of the superficial aponeurosis elongation on the whole muscle behavior.     

Tensile properties of the in vivo human gastrocnemius tendon

In the present experiment we obtained the tensile properties of the human gastrocnemius tendon, a high-stressed tendon suitable for spring-like action during locomotion. Measurements were taken in vivo in six men. The gastrocnemius tendon elongation during tendon loading−unloading induced by muscle contraction−relaxation was measured using real-time ultrasonography. Tendon forces were calculated from the moment generated during isometric plantarflexion contraction, using tendon moment arm length data obtained in vivo with the tendon travel method. Tendon stiffness data were calculated from the slope of the tendon force−elongation curve, and were then normalized to the tendon's original dimensions, obtained from morphometric analysis of sonographs, to estimate the tendon Young's modulus. Mechanical hysteresis values were obtained from area calculations by numerical integration. The elongation of the tendon increased curvilinearly with the force acting upon it, from 1.7±1 mm (0.8±0.3% strain) at 87.5±8.5 N to 11.1±3.1 mm (4.9±1% strain) at 875±85 N. The tendon Young's modulus and mechanical hysteresis were 1.16±0.15 GPa and 18±3%, respectively. These values fall within the range of values obtained from in vitro experiments and are very similar to the respective values recently obtained from in vivo measurements in the less highly stressed human tibialis anterior tendon (1.2 GPa and 19%), thus indicating that the material properties of tendon are independent of physiological loading and function. Combining the present tendon force−elongation data with previously reported Achilles tendon force data recorded during walking indicates that the gastrocnemius tendon would provide 6% of the total external work produced by the locomotor system. This estimate illustrates the contribution of passive elastic mechanisms on the economy and efficiency of walking. The contributions would be greater in more active exercise such as running.     

Ultrasound estimates of Achilles tendon exhibit unexpected shortening during ankle plantarflexion

The purpose of this study was to investigate Achilles tendon (AT) length changes during a series of tasks that involved combinations of higher/lower force, and larger/smaller length changes of the medial gastrocnemius muscle-tendon unit (MTU). We sought to determine if common ultrasound-based estimates of AT length change were consistent with expectations for a passive elastic tendon acting in series with a muscle. We tested 8 healthy individuals during restricted joint calf contractions (high force, low displacement), ankle dorsi-/plantar-flexion (DF/PF) with the foot in the air (low force, high displacement), and heel raises (high force, high displacement). We experimentally estimated AT length change using two ultrasound methods, one based on muscle-tendon junction (MTJ) tracking and one based on muscle fascicle (MF) tracking. Estimates of AT length change were consistent with model expectations during restricted calf contractions, when the MTU underwent minimal length change. However, estimates of AT length changes were inconsistent with model expectations during the ankle DF/PF and heel raise tasks. Specifically, the AT was estimated to shorten substantially, often 10–20 mm, when the ankle plantarflexed beyond neutral position, despite loading conditions in which a passive, stiff spring would be expected to either lengthen (under increasing force) or maintain its length (under low force). These unexpected findings suggest the need for improvements in how we conceptually model and/or experimentally estimate MTU dynamics in vivo during motion analysis studies, particularly when the ankle plantarflexes beyond neutral.     

Mechanical properties of the gastrocnemius aponeurosis in wild turkeys

In many muscles, the tendinous structures include both an extramuscular free tendon as well as a sheet-like aponeurosis. In both free tendons and aponeuroses the collagen fascicles are oriented primarily longitudinally, along the muscle's line of action. It is generally assumed that this axis represents the direction of loading for these structures. This assumption is well founded for free tendons, but aponeuroses undergo a more complex loading regime. Unlike free tendons, aponeuroses surround a substantial portion of the muscle belly and are therefore loaded both parallel (longitudinal) and perpendicular (transverse) to a muscle's line of action when contracting muscles bulge to maintain a constant volume. Given this biaxial loading pattern, it is critical to understand the mechanical properties of aponeuroses in both the longitudinal and transverse directions. In this study, we use uniaxial testing of isolated tissue samples from the aponeurosis of the lateral gastrocnemius of wild turkeys to determine mechanical properties of samples loaded longitudinally (along the muscle's line of action) and transversely (orthogonal to the line of action). We find that the aponeurosis has a significantly higher Young's modulus in the longitudinal than in the transverse direction. Our results also show that aponeuroses can behave as efficient springs in both the longitudinal and transverse directions, losing little energy to hysteresis. We also test the failure properties of aponeuroses to quantify the likely safety factor with which these structures operate during muscular force production. These results provide an essential foundation for understanding the mechanical function of aponeuroses as biaxially loaded biological springs.     

Effects of submaximal and maximal long-lasting contractions on the compliance of vastus lateralis tendon and aponeurosis in vivo

The present study investigated the effects of submaximal sustained and maximal repetitive contractions on the compliance of human vastus lateralis (VL) tendon and aponeurosis in vivo using two different fatiguing protocols. Twelve male subjects performed three maximum voluntary isometric contractions (MVC) of the knee extensors before and after two fatiguing protocols on a dynamometer. The first fatiguing protocol consisted of a long-lasting sustained isometric knee extension contraction at 25% MVC until failure (inability to hold the defined load). The second fatiguing protocol included long-lasting isokinetic (90°/s) knee extension contractions, where maximum moment was exerted and failure was proclaimed when this value fell below 70% of unfatigued maximum isokinetic moment. Ultrasonography was used to determine the elongation and strain of the VL tendon and aponeurosis. Muscle fatigue was indicated by a significant decrease in maximum resultant knee extension moment (p < 0.05) observed during the MVCs after both long-lasting contractions. No significant (p > 0.05) differences in elongation and strain of the VL tendon and aponeurosis were found, when compared every 300 N (tendon force) before and after the fatiguing protocols. The present data indicate, that the VL tendon and aponeurosis in vivo do not suffer from changes in the compliance neither after long-lasting static mechanical loading (strain ～3.2%) nor after long-lasting cyclic mechanical loading (strain 6.2–5.5%).     

Mechanical properties of aponeurosis and tendon of the cat soleus muscle during whole-muscle isometric contractions

Recent studies have suggested that the mechanical properties of aponeurosis are not similar to the properties of external tendon. In the present study, the lengths of aponeurosis, tendon, and muscle fascicles were recorded individually, using piezoelectric crystals attached to the surface of each structure during isometric contractions in the cat soleus muscle. We used a surgical microscope to observe the surface of the aponeurosis, which revealed a confounding effect on measures of aponeurosis length due to sliding of a thin layer of epimysium over the proximal aponeurosis. After correcting for this artifact, the stiffness computed for aponeurosis was similar to tendon, with both increasing from around 8 F₀/L_c (F₀ is maximum isometric force and L_c is tissue length) at 0.1 F₀ to 30 F₀/L_c at forces greater than 0.4 F₀. At low force levels only (0.1 F₀), aponeurotic stiffness increased somewhat as fascicle length increased. There was a gradient in the thickness of the aponeurosis along its length: its thickness was minimal at the proximal end and maximal at the distal end, where it converged to form the external tendon. This gradient in thickness appeared to match the gradient in tension transmitted along this structure. We conclude that the specific mechanical properties of aponeurosis are similar to those of tendon. © 1995 Wiley-Liss, Inc.     

Optimal muscle fascicle length and tendon stiffness for maximising gastrocnemius efficiency during human walking and running

Muscles generate force to resist gravitational and inertial forces and/or to undertake work, e.g. on the centre of mass. A trade-off in muscle architecture exists in muscles that do both; the fibres should be as short as possible to minimise activation cost but long enough to maintain an appropriate shortening velocity. Energetic cost is also influenced by tendon compliance which modulates the timecourse of muscle mechanical work. Here we use a Hill-type muscle model of the human medial gastrocnemius to determine the muscle fascicle length and Achilles tendon compliance that maximise efficiency during the stance phase of walking (1.2 m/s) and running (3.2 and 3.9 m/s). A broad range of muscle fascicle lengths (ranging from 45 to 70 mm) and tendon stiffness values (150-500 N/mm) can achieve close to optimal efficiency at each speed of locomotion; however, efficient walking requires shorter muscle fascicles and a more compliant tendon than running. The values that maximise efficiency are within the range measured in normal populations. A non-linear toe-region region of the tendon force-length properties may further influence the optimal values, requiring a stiffer tendon with slightly longer muscle fascicles; however, it does not alter the main results. We conclude that muscle fibre length and tendon compliance combinations may be tuned to maximise efficiency under a given gait condition. Efficiency is maximised when the required volume of muscle is minimised, which may also help reduce limb inertia and basal metabolic costs.     

Effect of ankle joint position and electrode placement on the estimation of the antagonistic moment during maximal plantarflexion.

During maximal efforts, antagonistic activity can significantly influence the joint moment. During maximal voluntary "isometric" contractions, certain joint rotation can not be avoided. This can influence the estimation of the antagonistic moment from the EMG activity. Our study aimed to quantify the influence on the calculated agonistic moment produced during maximal voluntary isometric plantarflexions (a) when estimating antagonistic moments at different ankle angles and (b) when placing the EMG electrodes at different portions over the m. tibialis anterior. Ten subjects performed maximal voluntary isometric plantarflexions at 90 degrees ankle angle. In order to estimate the antagonistic moment, submaximal isometric dorsiflexions were performed at various ankle angles. Moment and EMG signals from mm. triceps surae and tibialis anterior were measured. The RMS differences between plantarflexors moment calculated considering the antagonistic cocontraction estimated at the same ankle angle at which the maximal plantarflexion moment was achieved and at different ankle angles ranged from 0.10 to 2.94 Nm. The location of the electrodes led to greater RMS differences (2.35-5.18 Nm). In conclusion, an angle 10 degrees greater than the initial plantarflexion angle is enough to minimize the effect of the change in length of the m. tibialis anterior during the plantarflexion on the estimation of the plantarflexors moment. The localisation of the electrodes over the m. tibialis anterior can influence the estimation of its cocontraction during maximal plantarflexion efforts.     

Length-force characteristics of aponeurosis in passive muscle and during isometric and slow dynamic contractions of rat gastrocnemius muscle

Length-force characteristics of aponeurosis of rat gastrocnemius medialis muscle and achilles tendon were studied for passive and active muscle. Active muscle performed isometric as well as slow concentric and eccentric contractions at low velocity. For isometric conditions, different aponeurosis and tendon length-force characteristics were found between passive and active muscle: At comparable low levels of force longer aponeuroses were encountered in passive than in active muscle. Similar results were found for achilles tendon, but the magnitude of the length change involved was smaller than for aponeurosis. For active muscle, no differences of aponeurosis length- force characteristics could be distinguished between the isometric contractions and a slow concentric contraction. Indications that such differences of aponeurosis length-force characteristics may exist between slow concentric and eccentric contractions were found. It is concluded that, for gastrocnemius medialis muscle, aponeurosis and tendon length - force characteristics may be quite variable depending on recent history of muscle length and activity.     

Mechanomyogram amplitude vs. isometric ankle plantarflexion torque of human medial gastrocnemius muscle at different ankle joint angles

The purpose of this study was to investigate the influence of changes in ankle joint angle on the mechanomyogram (MMG) amplitude of the human medial gastrocnemius (MG) muscle during voluntary isometric plantarflexion contractions. Ten healthy individuals were asked to perform voluntary isometric contractions at six different contraction intensities (from 10% to 100%) and at three different ankle joint angles (plantarflexion of 26°; plantarflexion of 10°; dorsiflexion of 3°). MMG signals were recorded from the surface over the MG muscle, using a 3-axis accelerometer. The relations between root mean square (RMS) MMG and isometric plantarflexion torque at different ankle joint angles were characterized to evaluate the effects of altered muscle mechanical properties on RMS MMG.We found that the relation between RMS MMG and plantarflexion torque is changed at different ankle joint angles: RMS MMG increases monotonically with increasing the plantarflexion torque but decreases as the ankle joint became dorsiflexed. Moreover, RMS MMG shows a negative correlation with muscle length, with passive torque, and with maximum voluntary torque, which were all changed significantly at different ankle joint angles.Our findings demonstrate the potential effects of changing muscle mechanical properties on muscle vibration amplitude. Future studies are required to explore the major sources of this muscle vibration from the perspective of muscle mechanics and muscle activation level, attributable to changes in the neural command.     

Biceps femoris and semitendinosus tendon/aponeurosis strain during passive and active (isometric) conditions

The purpose of this study was to quantify strain and elongation of the long head of the biceps femoris (BFlh) and the semitendinosus (ST) tendon/aponeurosis. Forty participants performed passive knee extension trials from 90° of knee flexion to full extension (0°) followed by ramp isometric contractions of the knee flexors at 0°, 45° and 90° of knee flexion. Two ultrasound probes were used to visualize the displacement of BFlh and ST tendon/aponeurosis. Three-way analysis of variance designs indicated that: (a) Tendon/aponeurosis (passive) elongation and strain were higher for the BFlh than the ST as the knee was passively extended (p < 0.05), (b) contraction at each angular position was accompanied by a smaller BFlh tendon/aponeurosis (active) strain and elongation than the ST at higher levels of effort (p < 0.05) and (c) combined (passive and active) strain was significantly higher for the BFlh than ST during ramp contraction at 0° but the opposite was observed for the 45° and 90° flexion angle tests (p < 0.05). Passive elongation of tendon/aponeurosis has an important effect on the tendon/aponeurosis behavior of the hamstrings and may contribute to a different loading of muscle fibers and tendinous tissue between BFlh and ST.     

Comparison of elasticity of human tendon and aponeurosis in knee extensors and ankle plantar flexors in vivo

The purposes of this study were to compare the elasticity of tendon and aponeurosis in human knee extensors and ankle plantar flexors in vivo and to examine whether the maximal strain of tendon was correlated to that of aponeurosis. The elongation of tendon and aponeurosis during isometric knee extension (n = 23) and ankle plantar flexion (n = 22), respectively, were determined using a real-time ultrasonic apparatus, while the participants performed ramp isometric contractions up to voluntary maximum. To calculate the strain values from the measured elongation, we measured the respective length of tendon and aponeurosis. For the knee extensors, the maximal strain of aponeurosis (12.1 +/- 2.8 %) was significantly greater than that of the patella tendon (8.3 +/- 2.4 %), p < 0.001. On the contrary, the maximal strain of Achilles tendon (5.9 +/- 1.4 %) was significantly greater than that of aponeurosis in ankle plantar flexors (2.7 +/- 1.4 %), p < 0.001. Furthermore, for both knee extensors and ankle plantar flexors there was no significant correlation between maximal strain of tendon and aponeurosis. These results would be important for understanding the different roles of tendon and aponeurosis during human movements and for more accurate muscle modeling.     

Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort

The purpose of this study was to estimate the relative contributions of central and peripheral factors to the development of human muscle fatigue. Nine healthy subjects [five male, four female; age = 30 (2) years, mean (SE)] sustained a maximum voluntary isometric contraction (MVC) of the ankle dorsiflexor muscles for 4 min. Fatigue was quantitated as the fall in MVC. Three measures of central activation and one measure of peripheral activation (compound muscle action potential, CMAP) were made using electromyography (EMG) and electrical stimulation. Measures of intramuscular metabolism were made using magnetic resonance spectroscopy. After exercise, MVC and electrically stimulated tetanic contraction (50 Hz, 500 ms) forces were 22.2 (3.7)% and 37.3 (7.1)% of pre-exercise values, respectively. The measures of central activation suggested some central fatigue during exercise: (1) the central activation ratio [MVC/(MVC + superimposed tetanic force)] fell from 0.94 (0.03) to 0.78 (0.09), (2) the MVC/tetanic force ratio fell from 2.3 (0.7) to 1.3 (0.7), and (3) the integral of the EMG (iEMG) signal decreased to 72.6 (9.1)% of the initial value, while the CMAP amplitude was unchanged. Intramuscular pH was associated by regression with the decline in MVC force (and therefore fatigue) and iEMG. The results indicate that central factors, which were not associated with altered peripheral excitability, contributed approximately 20% to the muscle fatigue developed, with the remainder being attributable to intramuscular (i.e., metabolic) factors. The association between pH and iEMG is consistent with proton concentration as a feedback mechanism for central motor drive during maximal effort.     

Influence of tendon slack on electromechanical delay in the human medial gastrocnemius in vivo.

The purpose of this study was to clarify the influence of muscle-tendon complex stretch on electromechanical delay (EMD) in terms of the extent of tendon slack in the human medial gastrocnemius (MG). EMD and MG tendon length were measured at each of five ankle joint angles (-30, -20, -10, 0, and 5 degrees : positive values for dorsiflexion) using percutaneous electrical stimulation and ultrasonography, respectively. The extent of MG tendon slack was calculated as MG tendon length shortening, standardized with MG tendon slack length obtained at the joint angle (-16 degrees +/- 5 degrees ) where the passive ankle joint torque was zero. EMD at -30 degrees (19.2 +/-2.2 ms) and -20 degrees (17.2 +/- 1.3 ms) was significantly greater than that at -10 degrees (16.0 +/-2.3 ms), 0 degrees (15.0 +/-1.4 ms), and 5 degrees (14.8 +/-1.4 ms), and at 0 and 5 degrees, respectively. The relative EMD, normalized with the maximal EMD for each subject, decreased dependent on the extent of decrease in MG tendon slack. There were no significant differences in EMD among the joint angles (-10, 0, and 5 degrees ) where MG tendon slack was taken up. These results suggest that the extent of tendon slack is an important factor for determining EMD.     

Residual force enhancement during submaximal and maximal effort contractions of the plantar flexors across knee angle

Following active muscle lengthening, steady-state isometric force is elevated compared with an isometric contraction without prior lengthening for the same muscle length and activation level. This property of muscle contraction is known as residual force enhancement (RFE). Here, we aimed to determine whether neural factors may mask some of the mechanical benefits of RFE on plantar flexion torque production. Inherent to lengthening contractions is an increase in cortical and spinal-mediated inhibition, while knee flexion places the medial gastrocnemius at a neuromechanical disadvantage. Neuromuscular properties of the plantar flexors were investigated with a Humac Norm dynamometer in 10 males (∼27 years) with a flexed (90°) and extended (180°) knee and with or without calcaneal tendon vibration (frequency range: 80–110 Hz). There was no effect for vibration (p > 0.05), but there was an effect for knee angle (p < 0.05) such that there was a 2 fold increase in RFE with the knee flexed compared with extended. During submaximal torque matching, following active lengthening there was an activation reduction (electromyography; EMG) of 7.2 and 4.7% with the knee flexed and extended, respectively for soleus as compared with the reference isometric contraction, but no difference for the medial gastrocnemius. Despite attempting to excite Ia input onto the plantar flexor motor neuron pool, vibration had no influence on RFE. Surprisingly, RFE was elevated more for the knee flexed than extended, which was possibly owing to the activation differences across the disparate muscles of the triceps surae during the plantar flexion task.