Constantinos N. Maganaris

In vivo behaviour of human muscle tendon during walking.

In the present study we investigated in vivo length changes in the fascicles and tendon of the human gastrocnemius medialis (GM) muscle during walking. The experimental protocol involved real–time ultrasound scanning of the GM muscle, recording of the electrical activity of the muscle, measurement of knee– and ankle–joint rotations, and measurement of ground reaction forces in six men during walking at 3 km h–1 on a treadmill. Fascicular lengths were measured from the sonographs recorded. Musculotendon complex length changes were estimated from anatomical and joint kinematic data. Tendon length changes were obtained combining the musculotendon complex and fascicular length–change data. The fascicles followed a different length–change pattern from those of the musculotendon complex and tendon throughout the step cycle. Two important features emerged: (i) the muscle contracted near–isometrically in the stance phase, with the fascicles operating at ca. 50 mm; and (ii) the tendon stretched by ca. 7 mm during single support, and recoiled in push–off. The behaviour of the muscle in our experiment indicates consumption of minimal metabolic energy for eliciting the contractile forces required to support and displace the body. On the other hand, the spring–like behaviour of the tendon indicates storage and release of elastic–strain energy. Either of the two mechanisms would favour locomotor economy.

In vivo human tendon mechanical properties

1 The aim of the present study was to measure the mechanical properties of human tibialis anterior (TA) tendon in vivo. 2 Measurements were taken in five males at the neutral ankle position and involved: (a) isometric dynamometry upon increasing the voltage of percutaneous electrical stimulation of the TA muscle, (b) real‐time ultrasonography for measurements of the TA tendon origin displacement during contraction and tendon cross‐sectional area, and (c) magnetic resonance imaging for estimation of the TA tendon length and moment arm. 3 From the measured joint moments and estimated moment arms, the values of tendon force were calculated and divided by cross‐sectional area to obtain stress values. The displacements of the TA tendon origin from rest to all contraction intensities were normalized to tendon length to obtain strain values. From the data obtained, the tendon force‐displacement and stress‐strain relationships were determined and the tendon stiffness and Youngs modulus were calculated. 4 Tendon force and stress increased curvilinearly as a function of displacement and strain, respectively. The tendon force and displacement at maximum isometric load were 530 N and 4·1 mm, and the corresponding stress and strain values were 25 MPa and 2·5%, respectively. The tendon stiffness and Youngs modulus at maximum isometric load were 161 N mm−1 and 1·2 GPa, respectively. These results are in agreement with previous reports on in vitro testing of isolated tendons and suggest that under physiological loading the TA tendon operates within the elastic ‘toe’ region.

Effect of strength training on human patella tendon mechanical properties of older individuals

This study investigated the effect of strength training on the mechanical properties of the human patella tendon of older individuals. Subjects were assigned to training (n= 9; age 74.3 ± 3.5 years, body mass 69.7 ± 14.8 kg and height 163.4 ± 9.1 cm, mean ±s.d.) and control (n= 9; age 67.1 ± 2 years, body mass 73.5 ± 14.9 kg and height 168.3 ± 11.5 cm) groups. Strength training (two series of 10 repetitions at 80 % of five‐repetition maximum) was performed three times per week for 14 weeks using leg extension and leg press exercises. Measurements of tendon elongation during a ramp isometric knee extension were performed before and after training and control periods in vivo using ultrasonography. Training caused a decreased tendon elongation and strain at all levels of force and stress (P < 0.01). Baseline tendon elongation and strain at maximal tendon load were 4.7 ± 1.1 mm and 9.9 ± 2.2 %, respectively (maximum force: 3346 ± 1168 N; maximum stress: 40 ± 11 MPa). After training, these values decreased to 2.9 ± 1.2 mm and 5.9 ± 2.4 % (P < 0.01), respectively (maximum force: 3555 ± 1257 N; maximum stress: 42 ± 11 MPa). Tendon stiffness increased by 65 % (2187 ± 713 to 3609 ± 1220 N mm−1; P < 0.05) and Youngs modulus increased by 69 % (1.3 ± 0.3 to 2.2 ± 0.8 GPa; P < 0.01). As a result of these changes, the rate of torque development increased by 27 % (482.8 ± 302.5 to 612.6 ± 401 N m s−1; P < 0.01) following training. No significant changes occurred in any measured variables in the control group (P > 0.05). This study shows for the first time that strength training in old age increases the stiffness and Youngs modulus of human tendons. This may reduce the risk of tendon injury in old age and has implications for contractile force production and the rapid execution of motor tasks.

In vivo measurements of the triceps surae complex architecture in man: implications for muscle function

1 The objectives of this study were to (1) quantify experimentally in vivo changes in pennation angle, fibre length and muscle thickness in the triceps surae complex in man in response to changes in ankle position and isometric plantarflexion moment and (2) compare changes in the above muscle architectural characteristics occurring in the transition from rest to a given isometric plantarflexion intensity with the estimations of a planimetric muscle model assuming constant thickness and straight muscle fibres. 2 The gastrocnemius medialis (GM), gastrocnemius lateralis (GL) and soleus (SOL) muscles of six males were scanned with ultrasonography at different sites along and across the muscle belly at rest and during maximum voluntary contraction (MVC) trials at ankle angles of −15 deg (dorsiflexed direction), 0 deg (neutral position), +15 deg (plantarflexed direction) and +30 deg. Additional images were taken at 80, 60, 40 and 20 % of MVC at an ankle angle of 0 deg. 3 In all three muscles and all scanned sites, as ankle angle increased from −15 to +30 deg, pennation increased (by 6–12 deg, 39–67 %, P < 0.01 at rest and 9–16 deg, 29–43 %, P < 0.01 during MVC) and fibre length decreased (by 15–28 mm, 32–34 %, P < 0.01 at rest and 8–10 mm, 27–30 %, P < 0.05 during MVC). Thickness in GL and SOL increased during MVC compared with rest (by 5–7 mm, 36–47 %, P < 0.01 in GL and 6–7 mm, 38–47 %, P < 0.01 in SOL) while thickness of GM did not differ (P > 0.05) between rest and MVC. 4 At any given ankle angle the model underestimated changes in GL and SOL occurring in the transition from rest to MVC in pennation angle (by 9–12 deg, 24–38 %, P < 0.01 in GL and 9–14 deg, 25–28 %, P < 0.01 in SOL) and fibre length (by 6–15 mm, 22–39 %, P < 0.01 in GL and 6–8 mm, 23–24 %, P < 0.01 in SOL). 5 The findings of the study indicate that the mechanical output of muscle as estimated by the model used may be unrealistic due to errors in estimating the changes in muscle architecture during contraction compared with rest.

Ultrasonographic assessment of human skeletal muscle size.

The measurement of human muscle size is essential when assessing the effects of training, disuse and ageing. The considered ‘gold standard’ for cross-sectional area measurements of muscle size is magnetic resonance imaging (MRI). However, MRI is costly and often inaccessible. The aim of the present study was to test the reproducibility and validity of a more accessible alternative method using ultrasonography (ULT). We examined the cross-sectional areas in the vastus lateralis muscle of six individuals. Axial-plane ULT scans were taken at given levels along the entire muscle length. The ULT scanning was repeated on different days (reliability) and validated against MRI-based measurements. Mean intraclass correlation coefficients were 0.998 for the reliability of ULT and 0.999 for the validity of ULT against MRI. The coefficient of variation values for cross-sectional area measurements assessed by six different experimenters were 2.1% and 0.8% for images obtained with ULT and MRI, respectively. The ULT method is a valid and reliable alternative tool for assessing cross-sectional areas of large individual human muscles. The present findings justify the application of the ULT method for the detection of changes throughout large muscles in response to training, disuse or as a consequence of sarcopenia.

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 tendons original dimensions, obtained from morphometric analysis of sonographs, to estimate the tendon Youngs 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+/-1mm (0.8+/-0.3% strain) at 87.5+/-8.5 N to 11.1+/-3.1mm (4.9+/-1% strain) at 875+/-85 N. The tendon Youngs 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 approximately 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.

Human postural sway results from frequent, ballistic bias impulses by soleus and gastrocnemius

It has been widely assumed for nearly a century, that postural muscles operate in a spring‐like manner and that muscle length signals joint angle (the mechano‐reflex mechanism). Here we employ automated analysis of ultrasound images to resolve calf muscle (soleus and gastrocnemius) length changes as small as 10 μm in standing subjects. Previously, we have used balancing of a real inverted pendulum to make predictions about human standing. Here we test and confirm these predictions on 10 subjects standing quietly. We show that on average the calf muscles are actively adjusted 2.6 times per second and 2.8 times per unidirectional sway of the body centre of mass (CoM). These alternating, small (30–300 µm) movements provide impulsive, ballistic regulation of CoM movement. The timing and pattern of these adjustments are consistent with multisensory integration of all information regarding motion of the CoM, pattern recognition, prediction and planning using internal models and are not consistent with control solely by local reflexes. Because the system is unstable, errors in stabilization provide a perturbation which grows into a sway which has to be reacted to and corrected. Sagittal sway results from this impulsive control of calf muscle activity rather than internal sources (e.g. the heart, breathing). This process is quite unlike the mechano‐reflex paradigm. We suggest that standing is a skilled, trial and error activity that improves with experience and is automated (possibly by the cerebellum). These results complement and extend our recent demonstration that paradoxical muscle movements are the norm in human standing.

Human tendon behaviour and adaptation, in vivo

Tendon properties contribute to the complex interaction of the central nervous system, muscle–tendon unit and bony structures to produce joint movement. Until recently limited information on human tendon behaviour in vivo was available; however, novel methodological advancements have enabled new insights to be gained in this area. The present review summarizes the progress made with respect to human tendon and aponeurosis function in vivo, and how tendons adapt to ageing, loading and unloading conditions. During low tensile loading or with passive lengthening not only the muscle is elongated, but also the tendon undergoes significant length changes, which may have implications for reflex responses. During active loading, the length change of the tendon far exceeds that of the aponeurosis, indicating that the aponeurosis may more effectively transfer force onto the tendon, which lengthens and stores elastic energy subsequently released during unloading, in a spring‐like manner. In fact, data recently obtained in vivo confirm that, during walking, the human Achilles tendon provides elastic strain energy that can decrease the energy cost of locomotion. Also, new experimental evidence shows that, contrary to earlier beliefs, the metabolic activity in human tendon is remarkably high and this affords the tendon the ability to adapt to changing demands. With ageing and disuse there is a reduction in tendon stiffness, which can be mitigated with resistance exercises. Such adaptations seem advantageous for maintaining movement rapidity, reducing tendon stress and risk of injury, and possibly, for enabling muscles to operate closer to the optimum region of the length–tension relationship.

The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse.

We hypothesized that rates of myofibrillar and patellar tendon collagen synthesis would fall over time during disuse, the changes being accompanied in muscle by decreases in focal adhesion kinase (FAK) phosphorylation and in gene expression for proteolytic enzymes. We studied nine men (22 ± 4 years, BMI 24 ± 3 kg m−2 (means ±s.d.) who underwent unilateral lower leg suspension for 23 days; five were studied between 0 and 10 days and four between 10 and 21 days. Muscle and tendon biopsies were taken in the postabsorptive state at days 0, 10 and 21 for measurement of protein synthesis, gene expression and protein phosphorylation. Muscle cross‐sectional area decreased by 5.2% at 14 days and 10.0% (both P < 0.001), at 23 days, i.e. 0.5% day−1, whereas tendon dimensions were constant. Rates of myofibrillar protein synthesis fell (P < 0.01) from 0.047% h−1 at day 0 to 0.022% h−1 at 10 days without further changes. Tendon collagen synthetic rates also fell (P < 0.01), from 0.052 to 0.023% h−1 at 10 days and then to 0.010% h−1 at 21 days. FAK phosphorylation decreased 30% (P < 0.01) at 10 days. No changes occurred in the amounts/phosphorylation of PKB–P70s6k–mTOR pathway components. Expression of mRNA for MuRF‐1 increased ∼3‐fold at 10 days without changes in MAFbx or tripeptidyl peptidase II mRNA, but all decreased between 10 and 21 days. Thus, both myofibrillar and tendon protein synthetic rates show progressive decreases during 21 days of disuse; in muscle, this is accompanied by decreased phosphorylation of FAK, with no marked increases in genes for proteolytic enzymes.

Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men.

Muscles and tendons are highly adaptive to changes in chronic loading, though little is known about the adaptative time course. We tested the hypothesis that, in response to unilateral lower limb suspension (ULLS), the magnitude of tendon mechanical adaptations would match or exceed those of skeletal muscle. Seventeen men (1.79 ± 0.05 m, 76.6 ± 10.3 kg, 22.3 ± 3.8 years) underwent ULLS for 23 days (n= 9) or acted as controls (n= 8). Knee extensor (KE) torque, voluntary activation (VA), cross‐sectional area (CSA) (by magnetic resonance imaging), vastus lateralis fascicle length (Lf) and pennation angle (θ), patellar tendon stiffness and Youngs modulus (by ultrasonography) were measured before, during and at the end of ULLS. After 14 and 23 days (i) KE torque decreased by 14.8 ± 5.5% (P < 0.001) and 21.0 ± 7.1% (P < 0.001), respectively; (ii) VA did not change; (iii) KE CSA decreased by 5.2 ± 0.7% (P < 0.001) and 10.0 ± 2.0% (P < 0.001), respectively; Lf decreased by 5.9% (n.s.) and 7.7% (P < 0.05), respectively, and θ by 3.2% (P < 0.05) and 7.6% (P < 0.01); (iv) tendon stiffness decreased by 9.8 ± 8.2% (P < 0.05) and 29.3 ± 11.5% (P < 0.005), respectively, and Youngs modulus by 9.2 ± 8.2% (P < 0.05) and 30.1 ± 11.9% (P < 0.01), respectively, with no changes in the controls. Hence, ULLS induces rapid losses of KE muscle size, architecture and function, but not in neural drive. Significant deterioration in tendon mechanical properties also occurs within 2 weeks, exacerbating in the third week of ULLS. Rehabilitation to limit muscle and tendon deterioration should probably start within 2 weeks of unloading.