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Training-induced increase in Achilles tendon stiffness affects tendon strain pattern during running
(2019)
Amelie Werkhausen
; Neil J. Cronin
; Kirsten Albracht
; Gøran Paulsen
; Askild V. Larsen
; Jens Bojsen-Møller
; Olivier R. Seynnes
Background
During the stance phase of running, the elasticity of the Achilles tendon enables the utilisation of elastic energy and allows beneficial contractile conditions for the triceps surae muscles. However, the effect of changes in tendon mechanical properties induced by chronic loading is still poorly understood. We tested the hypothesis that a training-induced increase in Achilles tendon stiffness would result in reduced tendon strain during the stance phase of running, which would reduce fascicle strains in the triceps surae muscles, particularly in the mono-articular soleus.
Methods
Eleven subjects were assigned to a training group performing isometric singleleg plantarflexion contractions three times per week for ten weeks, and another ten subjects formed a control group. Before and after the training period, Achilles tendon stiffness was estimated, and muscle-tendon mechanics were assessed during running at preferred speed using ultrasonography, kinematics and kinetics.
Results
Achilles tendon stiffness increased by 18% (P <0:01) in the training group, but the associated reduction in strain seen during isometric contractions was not statistically significant. Tendon elongation during the stance phase of running was similar after training, but tendon recoil was reduced by 30% (P <0:01), while estimated tendon force remained unchanged. Neither gastrocnemius medialis nor soleus fascicle shortening during stance was affected by training.
Discussion
These results show that a training-induced increase in Achilles tendon
stiffness altered tendon behaviour during running. Despite training-induced changes in tendon mechanical properties and recoil behaviour, the data suggest that fascicle shortening patterns were preserved for the running speed that we examined. The asymmetrical changes in tendon strain patterns supports the notion that simple inseries models do not fully explain the mechanical output of the muscle-tendon unit during a complex task like running.
Dieter Blottner
; Maria Hastermann
; Paul Muckelt
; Kirsten Albracht
; Britt Schoenrock
; Michele Salanova
; Martin Warner
; Hans-Christian Gunga
; Maria Stokes
The MYOTONES experiment is the first to monitor changes in the basic biomechanical properties (tone, elasticity and stiffness) of the resting human myofascial system due to microgravity with a oninvasive, portable device on board the ISS. The MyotonPRO device applies several brief mechanical stimuli to the surface of the skin, and the natural oscillation signals of the tissue beneath are detected and computed by the MyotonPRO. Thus, an objective, quick and easy determination of the state of the underlying tissue is possible.
Two preflight, four inflight and four post flight measurements were performed on a male astronaut using the same 10 measurement points (MP) for each session. MPs were located on the plantar fascia, Achilles tendon, M. soleus, M. gastrocnemius, M. multifidus, M. splenius capitis, M. deltoideus anterior, M. rectus femoris, infrapatellar tendon, M. tibialis anterior. Subcutaneous tissues thickness above the MPs was measured using ultrasound imaging. Magnetic resonance images (MRI) of lower limb muscles and functional tests were also performed pre- and postflight.
Our first measurements on board the ISS confirmed increased tone and stiffness of the lumbar multifidus muscle, an important trunk stabilizer, dysfunction of which is known to be associated with back pain. Furthermore, reduced tone and stiffness of Achilles tendon and plantar fascia were observed inflight vs. preflight, confirming previous findings from terrestrial analog studies and parabolic
flights. Unexpectedly, the deltoid showed negative inflight changes in tone and stiffness, and increased elasticity, suggesting a potential risk of muscle atrophy in longer spaceflight that should be addressed by adequate inflight countermeasure protocols. Most values from limb and back MPS showed deflected patterns (in either directions) from inflight shortly after the re-entry phase on the landing day and one week later. Most parameter values then normalized to baseline after 3 weeks likely due to 1G re-adaptation and possible outcome of the reconditioning protocol. No major changes in subcutaneous tissues thickness above the MPs were found inflight vs preflight, suggesting no bias (i.e., fluid shift, extreme tissue thickening or loss). Pre- and postflight MRI and functional tests showed negligible changes in calf muscle size, power and force, which is likely due to training effects from current inflight exercise protocols.
The MYOTONES experiment is currently ongoing to collect data from further crew members. The potential impact of this research is to better understand the effects of microgravity and countermeasures over the time course of an ISS mission cycle. This will enable exercise countermeasures to be tailored
Effective training requires high muscle forces potentially leading to training-induced injuries. Thus, continuous monitoring and controlling of the loadings applied to the musculoskeletal system along the motion trajectory is required. In this paper, a norm-optimal iterative learning control algorithm for the robot-assisted training is developed. The algorithm aims at minimizing the external knee joint moment, which is commonly used to quantify the loading of the medial compartment. To estimate the external knee joint moment, a musculoskeletal lower extremity model is implemented in OpenSim and coupled with a model of an industrial robot and a force plate mounted at its end-effector. The algorithm is tested in simulation for patients with varus, normal and valgus alignment of the knee. The results show that the algorithm is able to minimize the external knee joint moment in all three cases and converges after less than seven iterations.
Neuromuscular strength training of the leg extensor muscles plays an important role in the rehabilitation and prevention of age and wealth related diseases. In this paper, we focus on the design and implementation of a Cartesian admittance control scheme for isotonic training, i.e. leg extension and flexion against a predefined weight. For preliminary testing and validation of the designed algorithm an experimental research and development platform consisting of an
industrial robot and a force plate mounted at its end-effector has been used. Linear, diagonal and arbitrary two-dimensional motion trajectories with different weights for the leg extension and flexion part are applied. The proposed algorithm is easily adaptable to trajectories consisting of arbitrary six-dimensional poses and allows the implementation of individualized trajectories.
To prevent the reduction of muscle mass and loss of strength coming along with the human aging process, regular training with e.g. a leg press is suitable. However, the risk of training-induced injuries requires the continuous monitoring and controlling of the forces applied to the musculoskeletal system as well as the velocity along the motion trajectory and the range of motion. In this paper, an adaptive norm-optimal iterative learning control algorithm to minimize the knee joint loadings during the leg extension training with an industrial robot is proposed. The response of the algorithm is tested in simulation for patients with varus, normal and valgus alignment of the knee and compared to the results of a higher-order iterative learning control algorithm, a robust iterative learning control and a recently proposed conventional norm-optimal iterative learning control algorithm. Although significant improvements in performance are made compared to the conventional norm-optimal iterative learning control algorithm with a small learning factor, for the developed approach as well as the robust iterative learning control algorithm small steady state errors occur.
Benjamin Stäudle
; Olivier Seynnes
; Guido Laps
; Fabian Göll
; Gert-Peter Brüggemann
; Kirsten Albracht
Achilles tendon rupture (ATR) patients have persistent functional deficits in the triceps surae muscle–tendon unit (MTU). The complex remodeling of the MTU accompanying these deficits remains poorly understood. The purpose of the present study was to associate in vivo and in silico data to investigate the relations between changes inMTU properties and strength deficits inATR patients. Methods: Elevenmale subjects who had undergone surgical repair of complete unilateral ATR were examined 4.6 ± 2.0 (mean ± SD) yr after rupture. Gastrocnemius medialis (GM) tendon stiffness, morphology, and muscle architecture were determined using ultrasonography. The force–length relation of the plantar flexor muscles was assessed at five ankle joint angles. In addition, simulations (OpenSim) of the GM MTU force–length properties were performed with various iterations of MTU properties found between the unaffected and the affected side. Results: The affected side of the patients displayed a longer, larger, and stiffer GM tendon (13% ± 10%, 105% ± 28%, and 54% ± 24%, respectively) compared with the unaffected side. The GM muscle fascicles of the affected side were shorter (32% ± 12%) and with greater pennation angles (31% ± 26%). A mean deficit in plantarflexion moment of 31% ± 10% was measured. Simulations indicate that pairing an intact muscle with a longer tendon shifts the optimal angular range of peak force outside physiological angular ranges, whereas the shorter muscle fascicles and tendon stiffening seen in the affected side decrease this shift, albeit incompletely. Conclusions: These results suggest that the substantial changes in MTU properties found in ATR patients may partly result from compensatory remodeling, although this process appears insufficient to fully restore muscle function.
Elena Monti
; Janice Waldvogel
; Ramona Ritzmann
; Kathrin Freyler
; Kirsten Albracht
; Michael Helm
; Niccolò De Cesare
; Piero Pavan
; Carlo Reggiani
; Albert Gollhofer
; Marco Vincenzo Narici
Performing tasks, such as running and jumping, requires activation of the agonist and antagonist muscles before (motor unit pre-activation) and during movement performance (Santello and Mcdonagh, 1998). A well-timed and regulated muscle activation elicits a stretch-shortening cycle (SSC) response, naturally occurring in bouncing movements (Ishikawa and Komi, 2004; Taube et al., 2012). By definition, the SSC describes the stretching of a pre-activated muscle-tendon complex immediately followed by a muscle shortening in the concentric push-off phase (Komi, 1984).
Given the importance of SSC actions for human movement, it is not surprising that many studies investigated the biomechanics of this phenomenon; in particular, drop jumps (DJs) represent a good paradigm to study muscle fascicle and tendon behavior in ballistic movements involving the SSC.
Within a DJ, three main phases [pre-activation, braking, and push-off (PO; Komi, 2000)] have been recognized and extensively studied in common and challenging conditions, such as changes in load, falling height, or simulated hypo-gravity (Avela et al., 1994; Arampatzis et al., 2001; Fukashiro et al., 2005; Ishikawa et al., 2005; Sousa et al., 2007; Ritzmann et al., 2016; Helm et al., 2020).
These studies show that the timing and amount of triceps-surae muscle-tendon unit pre-activation in DJs are differentially regulated based on the load applied to the muscle, being optimal in normal “Earth” gravity conditions (Avela et al., 1994), but decreased in simulated hypo-gravity, hyper-gravity (Avela et al., 1994; Ritzmann et al., 2016), or unknown conditions (i.e., unknown falling heights; Helm et al., 2020). Some authors indicated that, when falling from heights different from the optimal one [defined as the drop height giving a maximum DJ performance indicated as peak ground reaction force (GRF) or jump high], electromyographic (EMG) activity of the plantar flexors increases from lower than optimal to higher than optimal heights (Ishikawa and Komi, 2004; Sousa et al., 2007).
These findings highlight the ability of the central nervous system to regulate the timing and amount of pre-activation according to different jumping conditions, thus regulating muscle fascicle length, tendon and joint stiffness as well as position, in order to safely land on the ground and quickly re-bounce.
Similarly, to pre-activation, also in the braking phase, the plantar flexors are differentially regulated. In optimal height (i.e., load) jumping conditions, gastrocnemius medialis (GM) fascicles shorten at early ground contact (possibly due to the intervention of the stretch reflex; Gollhofer et al., 1992) and behave quasi-isometrically in the late braking phase, enabling tendon elongation, and storage of elastic energy (Gollhofer et al., 1992; Fukashiro et al., 2005; Sousa et al., 2007). When increasing the falling height (augmenting the impact GRF), the quasi-isometric behavior of fascicles disappears, and fast fascicle lengthening occurs (Ishikawa et al., 2005; Sousa et al., 2007).
In the third and last PO phase, fascicles shorten and the tendon releases the elastic energy previously stored. Bobbert et al. (1987) reported no influence of jumping height on the work done and on the net vertical impulse assessed during PO; this observation suggests that, despite an optimal DJ performance might be achieved only in specific conditions (falling heights, loads), the central nervous system seems to be able to regulate muscle behavior in order to effectively perform the required task also in challenging situations.
Although the regulation of triceps-surae muscle-tendon unit in DJs has been extensively investigated, very few studies focused on sarcomeres behavior during the performance of this SSC movement (Kurokawa et al., 2003; Fukashiro et al., 2005, 2006). Sarcomeres represent muscle contractile units and are known to express different amounts of force depending on their length (Gordon et al., 1966; Walker and Schrodt, 1974); thus, understanding the time course of their responses during DJs is fundamental to gain further insights into muscle force-generating capacity. In vivo measurement of sarcomere length in humans has been so far been performed only in static positions and under highly controlled experimental conditions (Llewellyn et al., 2008; Sanchez et al., 2015). Instead, human sarcomere length estimation (achieved by dividing GM measured fascicle length for a fixed sarcomere number) in dynamic contractions provided an indirect measure of sarcomere operating range during squat jump, countermovement jump, and DJ (Fukashiro et al., 2005, 2006; Kurokawa et al., 2003). The results of these studies showed that sarcomeres operate in the ascending limb of their length-tension (L-T) relationship in all types of jumps, and particularly so in DJ.
However, most of the available observations on sarcomere and muscle fascicle behavior were made in condition of constant gravity. Thus, in order to understand how sarcomere and muscle fascicle length are regulated in variable gravity conditions, we performed experiments in a parabolic flight, involving variable gravity levels, ranging from about zero-g to about double the Earth’s gravity (1 g; Waldvogel et al., 2021).
Specifically, the aims of the present study were as follows:
1. To investigate the ability of the neuromuscular system in regulating fascicle length in response to conditions of variable gravity.
2. To estimate sarcomere operative length in the different DJ phases, in order to calculate its theoretical force production and its possible modulation in conditions of variable gravity.
We hypothesized that muscle fascicles would be differentially regulated in different gravity conditions compared to 1 g, particularly in anticipation of landing and re-bouncing in unknown gravity levels. In addition, we hypothesized that sarcomeres would operate in the upper part of the ascending limb of their L-T relationship, possibly lengthening during the braking phase (especially in hyper-gravity) while operating quasi-isometrically in 1 g.
The compliant nature of distal limb muscle-tendon units is traditionally considered suboptimal in explosive movements when positive joint work is required. However, during accelerative running, ankle joint net mechanical work is positive. Therefore, this study aims to investigate how plantar flexor muscle-tendon behavior is modulated during fast accelerations. Eleven female sprinters performed maximum sprint accelerations from starting blocks, while gastrocnemius muscle fascicle lengths were estimated using ultrasonography. We combined motion analysis and ground reaction force measurements to assess lower limb joint kinematics and kinetics, and to estimate gastrocnemius muscle-tendon unit length during the first two acceleration steps. Outcome variables were resampled to the stance phase and averaged across three to five trials. Relevant scalars were extracted and analyzed using one-sample and two-sample t-tests, and vector trajectories were compared using statistical parametric mapping. We found that an uncoupling of muscle fascicle behavior from muscle-tendon unit behavior is effectively used to produce net positive mechanical work at the joint during maximum sprint acceleration. Muscle fascicles shortened throughout the first and second steps, while shortening occurred earlier during the first step, where negative joint work was lower compared with the second step. Elastic strain energy may be stored during dorsiflexion after touchdown since fascicles did not lengthen at the same time to dissipate energy. Thus, net positive work generation is accommodated by the reuse of elastic strain energy along with positive gastrocnemius fascicle work. Our results show a mechanism of how muscles with high in-series compliance can contribute to net positive joint work.
Charlotte Richter
; Björn Braunstein
; Benjamin Stäudle
; Julia Attias
; Alexander Süss
; Tobias Weber
; Katya N. Mileva
; Jörn Rittweger
; David A. Green
; Kirsten Albracht
The international partnership of space agencies has agreed to proceed forward to the Moon sustainably. Activities on the Lunar surface (0.16 g) will allow crewmembers to advance the exploration skills needed when expanding human presence to Mars (0.38 g). Whilst data from actual hypogravity activities are limited to the Apollo missions, simulation studies have indicated that ground reaction forces, mechanical work, muscle activation, and joint angles decrease with declining gravity level. However, these alterations in locomotion biomechanics do not necessarily scale to the gravity level, the reduction in gastrocnemius medialis activation even appears to level off around 0.2 g, while muscle activation pattern remains similar. Thus, it is difficult to predict whether gastrocnemius medialis contractile behavior during running on Moon will basically be the same as on Mars. Therefore, this study investigated lower limb joint kinematics and gastrocnemius medialis behavior during running at 1 g, simulated Martian gravity, and simulated Lunar gravity on the vertical treadmill facility. The results indicate that hypogravity-induced alterations in joint kinematics and contractile behavior still persist between simulated running on the Moon and Mars. This contrasts with the concept of a ceiling effect and should be carefully considered when evaluating exercise prescriptions and the transferability of locomotion practiced in Lunar gravity to Martian gravity.
This study aims to quantify the kinematics, kinetics and muscular activity of all-out handcycling exercise and examine their alterations during the course of a 15-s sprint test. Twelve able-bodied competitive triathletes performed a 15-s all-out sprint test in a recumbent racing handcycle that was attached to an ergometer. During the sprint test, tangential crank kinetics, 3D joint kinematics and muscular activity of 10 muscles of the upper extremity and trunk were examined using a power metre, motion capturing and surface electromyography (sEMG), respectively. Parameters were compared between revolution one (R1), revolution two (R2), the average of revolution 3 to 13 (R3) and the average of the remaining revolutions (R4). Shoulder abduction and internal-rotation increased, whereas maximal shoulder retroversion decreased during the sprint. Except for the wrist angles, angular velocity increased for every joint of the upper extremity. Several muscles demonstrated an increase in muscular activation, an earlier onset of muscular activation in crank cycle and an increased range of activation. During the course of a 15-s all-out sprint test in handcycling, the shoulder muscles and the muscles associated to the push phase demonstrate indications for short-duration fatigue. These findings are helpful to prevent injuries and improve performance in all-out handcycling.