Eur J Appl Physiol (2014) 114:1403–1411 DOI 10.1007/s00421-014-2871-4
Original Article
Changes in contractile and elastic properties of the triceps surae muscle induced by neuromuscular electrical stimulation training Jean‑Francois Grosset · Francis Canon · Chantal Pérot · Daniel Lambertz
Received: 15 November 2013 / Accepted: 5 March 2014 / Published online: 20 March 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose Neuromuscular electrical stimulation (NMES) training is known to induce improvement in force production capacities and fibre-type transition. The aim of this study was to determine whether NMES training also leads to changes in the mechanical properties of the human triceps surae (TS) muscle. Methods Fifteen young male subjects performed a training protocol (4 weeks, 18 sessions, 4–5 sessions per week) based on a high-frequency isometric NMES programme of TS muscle. Quick-release test was used to evaluate Musculo-Tendinous (MT) stiffness index (SIMT) as the slope of the linear MT stiffness–torque relationships under submaximal contraction. Sinusoidal perturbations allowed the assessment of musculo-articular stiffness index (SIMA) as well as the calculation of the maximal angular veloc′ ity (Θmax ) of TS muscle using an adaptation of Hill’s equation. Results After NMES training, Maximal Voluntary Con′ traction under isometric conditions and Θmax increased significantly by 17.5 and 20.6 %, respectively, while SIMT
and SIMA decreased significantly (−12.7 and −9.3 %, respectively). Conclusions These changes in contractile and elastic properties may lead to functional changes of particular interest in sport-related activities as well as in the elderly. Keywords Neuromuscular electrical simulation · Musculo-tendinous stiffness · Maximal angular velocity · Triceps surae · Training
J.-F. Grosset (*) · F. Canon · C. Pérot CNRS UMR 7338, Biomécanique et Bioingénierie, Université de Technologie de Compiègne, 60205 Compiègne cedex, France e-mail: [email protected]
Abbreviations α Torque constant β Angular velocity constant CSA Cross-sectional area Kopt Optimal angular stiffness Kp Passive musculo-articular Stiffness MHC Myosin heavy chain MVC Maximal voluntary contraction NMES Neuromuscular electrical stimulation ′ Θmax Maximal shortening/angular velocity (for in vivo muscle) ′ Optimal shortening/angular velocity Θopt SEC Series elastic component SIMA Musculo-articular stiffness index SIMT Musculo-tendinous stiffness index Topt Optimal torque Vmax Maximal shortening velocity (for isolated muscle) ωopt Optimal angular velocity
J.-F. Grosset UFR Santé Médecine et Biologie Humaine, Université Paris 13, Sorbonne Paris Cité, Bobigny, France
Introduction
D. Lambertz Departemento de Educacao Fisica e Ciencas do Esporte, Universidade Federal de Pernambuco-Centro Academico de Vitoria de Santo Antao, Vitoria de Santo Antao, Brazil
Neuromuscular electrical stimulation (NMES), used as strength training mode, is known to improve neuromuscular function in healthy individuals with an increase in
Communicated by Olivier Seynnes.
13
1404
maximal voluntary contraction (MVC) as the main result. This strength gain could be attributed to neural adaptations as well as muscular changes (see Hortobagyi and Maffiuletti (2011) for review). Furthermore, fibre-type transitions following an NMES training period in sedentary subjects have been reported. More precisely, Perez et al. (2002) reported a decrease in fibres expressing Myosin Heavy Chain (MHC) IIx and I to the profit of fibres expressing MHC IIa. Recently, Gondin et al. (2011) showed an increase in MHC IIa and MHC I in vastus lateralis of sedentary subjects after NMES to the detriment of MHC IIx. It can be assumed that changes in fibre-type proportion due to NMES training would have some mechanical implications. Indeed, the Series Elastic Component (SEC) is composed not only by a passive fraction located at the tendinous level but also by an active fraction located at the cross-bridge level. Thus, a link between fibre-type composition and Series Elastic Component (SEC) characteristics has been proposed (Bosco et al. 1982), slow-twitch motor units eliciting a greater SEC stiffness than fast-twitch ones (Petit et al. 1990). Moreover, in animals different training programmes have shown to induce paired changes in SEC properties and muscle fibres composition (Almeida-Silveira et al. 1994; Goubel and Marini 1987; Pousson et al. 1991). Endurance training induced a decrease in fast-twitch fibre proportion associated with an increase in the stiffness of the series elastic component (SEC) (Goubel and Marini 1987). In contrast, a plyometric training programme leads to an increase in the percentage of fast-twitch fibres associated to a decrease in SEC stiffness (Almeida-Silveira et al. 1994). In humans, Grosset et al. (2009) reported a decrease in SEC stiffness after plyometric training. Regarding the passive part of the SEC, it has not been shown changes in tendon stiffness following plyometric training (Foure et al. 2012; Kubo et al. 2007). Thus, the decrease in SEC stiffness observed after plyometric training is certainly only due to an increase in fast fibre proportion as in animal studies (Simoneau et al. 1985). Following endurance training the increase in SEC stiffness of the ankle plantar flexors (Grosset et al. 2009) is due to an increase in tendon stiffness (Kubo et al. 2001) as well as an increase in slowtwitch fibres as expected from animal studies (Goubel and Marini 1987). Another skeletal muscle adaptive response to changes in fibre-type profile can be evidenced through changes in maximal shortening velocity (Vmax). This characteristic is a function of myosin ATPase and correlation between Vmax and the percentage of fast MHC has been reported (Reiser et al. 1985). Thus, it has been shown that Vmax increased in parallel with an increase in fast-twitch fibre proportion in isolated soleus muscle after stretch–shortening cycle training in rats (Almeida-Silveira et al. 1996). In humans, using isokinetic contractions, Thorstensson et al. (1976) reported
13
Eur J Appl Physiol (2014) 114:1403–1411
correlations between peak torque at the highest speed of muscle shortening and percentage of fast-twitch fibre in knee extensor muscles. Moreover, Lambertz et al. (2001) reported an increase in maximal angular velocity index in plantar flexors after long-term spaceflight and ascribed this change in part to an increase in fast-twitch fibre percentage. To date, skeletal muscle contractile and elastic mechanical properties have never been investigated following highfrequency NMES training period. Thus, the aim of the present study is to quantify musculo-tendinous stiffness as well as maximal angular velocity of triceps surae muscle following a high-frequency NMES training programme. Maximal angular velocity will be assessed using sinusoidal perturbations technique proposed by Desplantez and Goubel (2002).
Methods Subjects The experiment was done on 15 volunteered sedentary college students (age 21.3 ± 0.3 years, stature 177.2 ± 4.3 cm, body mass 70.2 ± 3.4 kg). All the subjects were fully informed about the procedure and gave their informed consent. They were free to withdraw from the study at any time. Each subject was familiarized with the experiment during a preliminary session, one week before starting the pre-training tests. The experimental protocol was approved by the committee of hygiene, safety and ethics at the University of Technology of Compiègne and carried out in accordance with the declaration of Helsinki. All subjects were free from illness or injury. None of the study participants had previously been exposed to NMES or were engaged in systematic resistance training for 12 months or longer prior to taking part in this investigation. NMES training To apply an equivalent training load, based on training sessions number, as compared with previous studies (Gondin et al. 2011; Maffiuletti et al. 2002; Vaz et al. 2013), the subjects completed a 18 sessions of isometric NMES over 4 weeks (i.e. 4–5 sessions per week). Forty-five-induced maximal contractions of the left plantar flexor muscles were induced during each training session (duration ~25 min including warm-up). A standardized warm-up before each session consisted in 5 min of submaximal low-frequency NMES (5 Hz, pulse duration 350 μs). To receive NMES, subjects were comfortably seated with ankle, knee and hip at 90°. Leg and ankle motions were prevented thanks to a custom-made system firmly attached to the floor and positioned on the thigh to ensure standardized isometric
Eur J Appl Physiol (2014) 114:1403–1411
contractions of the plantar flexors throughout the training sessions. A portable stimulator (Compex Sport-P, Medicompex SA, Ecublens, Switzerland) was used to deliver biphasic symmetric rectangular pulses with the following characteristics: frequency 75 Hz, pulse duration 400 μs, 6.25 s on, 20 s off. Three 2-mm-thick self-adhesive electrodes were placed over the left leg. Two positive electrodes (5 × 5 cm) were positioned over the superficial aspect of the left soleus muscle, about 5 cm distal from where the medial and lateral heads of the gastrocnemius muscle join the Achilles tendon. The rectangular (10 × 5 cm) negative electrode was placed along the middorsal line of the leg, and over both medial and lateral gastrocnemius. Current intensity was gradually increased during NMES contractions until the maximally tolerated intensity depending on the subjects’ pain threshold. From one session to another, the maximally tolerated intensity was frequently increased due to subject’s habituation to NMES. The %MVC reached by each subject during NMES training sessions was not monitored in the present study. However, Maffiuletti et al. (2002) reported during a high-frequency NMES training of the triceps surae muscle that the subjects reached between 50 and 70 % MVC during the session. All NMES training sessions were supervised by one of the experimenters. Ergometric device Biomechanical tests were performed using an ankle ergometer (Tognella et al. 1997). The ergometer has two main parts: an electronic device and a mechanical device. The electronic device has a power unit, position and torque transducers and a driving unit equipped with a PC including a 12 bit A/D converter, three timers and a 16TTL output. The mechanical device consists of an actuator (Megatorque motor NSK RS 1010) and transducers: a strain gauge torque (FGP CD 1050) and a 12-bit optical shaft encoder (Hengstler RA 585). Specific menu-driven software controlled all procedures and permitted the simultaneous recording of mechanical signals (torque, angular displacement and angular velocity). A dual-beam oscilloscope gives the subject visual feedback about the procedure in progress. Mechanical tests Each subject sat on an armchair that could be adjusted vertically and horizontally. Dorsal support was provided during the rest periods, but not during voluntary contractions, to prevent extraneous movements and to limit the contribution of other muscles such as the trunk extensor muscles. The left foot was firmly held on to the footplate of the actuator so that the lateral malleolus coincided with the rotation axis of the actuator. The knee was extended to 120°
1405
(180° being full extension) and the ankle was placed at 90° (i.e. neutral position). A maximal voluntary contraction (MVC), corresponding to maximal isometric plantarflexion torque, was developed as fast as possible and maintained for 3 s. This was repeated three times, with 2 min of rest after each trial. The best of the three attempts gave the MVC for the day’s session. To avoid any-time-of-day effect on the investigated parameters, pre- and post-tests were performed at the same time of day (Castaingts et al. 2004; Martin et al. 1999). Elastic properties of the triceps surae musculo-tendinous (MT) complex were assessed by means of the quick-release technique adapted for in vivo experiments (Goubel and Pertuzon 1973). Quick-release movements were achieved around the neutral position by a sudden release of the footplate while the subject maintained a submaximal voluntary isometric torque in plantarflexion. Three attempts were performed at 20, 40, 60 and 80 % MVC, in a random order with 2 min rest between each trial. Then, sinusoidal oscillations (3° peak-to-peak) at different frequencies, ranging from 6 to 16 Hz, were imposed with 1 Hz step to characterize the mechanical properties of the musculo-articular (MA) system, while the subject maintained 20, 40 and 60 % MVC in plantarflexion. Sinusoidal perturbations at rest (i.e. 0 % MVC) were also performed. A 1-min rest interval was given between each trial. Data analysis Quick‑release test Musculo-tendinous stiffness was calculated as the ratio between variations in angular acceleration Θ¨ (as the second derivative of angular displacement, Θ) and angular displacement, multiplied by the corresponding inertia (I) over 20 ms after the sudden release of the footplate. Thus, this formula reads:
¨ S = (∆Θ/∆) ×I
(1)
Then, musculo-tendinous stiffness values were related to the corresponding isometric torque, calculated over the 200 ms that preceded the quick-release movement. The slope of the linear stiffness–torque relationship so obtained was defined as an index of the stiffness of the musculotendinous complex (SIMT). As such, SIMT was proposed to reflect changes in musculo-tendinous stiffness (Lambertz et al. 2001). Sinusoidal perturbations test The data processing for musculo-articular stiffness assessment has been previously reported by Lambertz et al. (2001). The MA elastic properties, including
13
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Eur J Appl Physiol (2014) 114:1403–1411
′ Fig. 1 Maximal angular velocity determination procedure (Θmax ) from sinusoidal perturbation test. In a stiffness–torque (filled square) and viscosity–torque relationships (unfilled circles) and their respective linear fit. Slope and intercept values are used to calculate α
parameter of Hills equation. In b Sinusoidal power–angular frequency (ω) relationship allowing the determination of angular frequency at maximal power (ωopt) used to determine β parameter of Hill’s equation
muscle–tendon and articular structures, were determined under passive (0 % of MVC) and active conditions (20, 40 and 60 % of MVC). Servo-controlled sinusoid length perturbations (3° peak-to-peak whatever the frequency of perturbations ranging from 6 to 16 Hz, see above) were used to establish frequency–response relationships (i.e. Bode diagrams), in which the averaged displacement-to-torque ratios and the phase shifts between displacement and torque were plotted against the imposed frequency. A Bode diagram reflects the mixed mechanical contribution of inertia (I), viscosity (B) and elasticity (K) according to the formula: Z(s) = I.s + B + K.s−1, where Z is the mechanical impedance and s is the Laplace operator. K and B values were calculated at 0, 20, 40 and 60 % MVC to construct the stiffness–torque or viscosity–torque relationships, respectively. Best fit for these relationships was obtained by a linear model: K = k1 T + k2, where T is the torque value, k1 the musculo-articular stiffness index, termed SIMA. k2 is the intercept point (IP). Musculo-articular stiffness in passive conditions was expressed by Kp, the stiffness at 0 % MVC. Finally, B was linearly related to torque to get a slope (b1) and intercept value (b2), as shown in Fig. 1a.
2002). An adaptation of Hill’s equation in terms of angular movements gives the following equation: (T + α) Θ ′ + β = (MVC + α)β (2)
Calculation of maximal angular velocity The hyperbolic relationship between force and velocity observed during isokinetic contraction was used to establish the so-called Hill’s equation [(P + a) (V + b) = (P0 + a)b] (b and a are, respectively, velocity and force constants of Hill’s equation, P is force developed at the shortening velocity V and P0 is tetanic force obtained under isometric condition), allowing assessment of the maximal angular velocity, i.e. the angular velocity at zero force. As in isokinetic condition, it is possible in vivo to evaluate maximal angular velocity at zero torque using sinusoidal perturbations technique (Desplantez and Goubel
13
where α and β are torque and angular velocity constants, respectively, T is torque, and Θ ′ is the angular velocity. Solving this equation when torque is zero allows the calcu′ lation of maximal angular velocity (Θmax ): ′ Θmax = MVC .β/α
(3)
The torque constant (α) can be calculated thanks to equation:
α = b2/b1,
(4)
where b1 and b2 are, respectively, slope and intercept of the viscosity–torque relationship (see Fig. 1a). Finally, the velocity constant (β) is determined with the following equation: ′ β = Θopt Topt + α / MVC − Topt , (5) ′ .is the optimal velocwhere Topt is optimal torque and Θopt ity [i.e. the torque and the velocity at maximal power developed during imposed pulsation (Fig. 1b)]. More details for the method can be found in Desplantez and Goubel (2002). From Eq. (2), the knowledge of α, β and MVC allows the establishment of the individual modelled torque–velocity relationship as well as the calculation of the maximal power (Pmax) and the corresponding torque and angular velocity values.
Statistics SigmaPlot 11.0 (Systat Software, San Jose, CA) was used to run statistical analyses. After a normality test
Eur J Appl Physiol (2014) 114:1403–1411
(Shapiro–Wilk test) validated for each of the investigated parameter, a Student’s t test for paired differences was used to test changes between pre- and post-NMES training protocol in all mechanical parameters (MVC, SIMT, SIMA, ′ Kp and Θmax ) due to NMES, as well as for all calculated ′ parameters necessary for Θmax estimation (Table 2). The level of significance was established at p ≤ 0.05. Values are presented as mean ± SD.
Results Mean maximal intensity applied by the subjects was significantly increased between the first and the fourth week of NMES training period ranging from 31.6 ± 8.7 to 94.1 ± 19.2 mA (p
Original Article
Changes in contractile and elastic properties of the triceps surae muscle induced by neuromuscular electrical stimulation training Jean‑Francois Grosset · Francis Canon · Chantal Pérot · Daniel Lambertz
Received: 15 November 2013 / Accepted: 5 March 2014 / Published online: 20 March 2014 © Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose Neuromuscular electrical stimulation (NMES) training is known to induce improvement in force production capacities and fibre-type transition. The aim of this study was to determine whether NMES training also leads to changes in the mechanical properties of the human triceps surae (TS) muscle. Methods Fifteen young male subjects performed a training protocol (4 weeks, 18 sessions, 4–5 sessions per week) based on a high-frequency isometric NMES programme of TS muscle. Quick-release test was used to evaluate Musculo-Tendinous (MT) stiffness index (SIMT) as the slope of the linear MT stiffness–torque relationships under submaximal contraction. Sinusoidal perturbations allowed the assessment of musculo-articular stiffness index (SIMA) as well as the calculation of the maximal angular veloc′ ity (Θmax ) of TS muscle using an adaptation of Hill’s equation. Results After NMES training, Maximal Voluntary Con′ traction under isometric conditions and Θmax increased significantly by 17.5 and 20.6 %, respectively, while SIMT
and SIMA decreased significantly (−12.7 and −9.3 %, respectively). Conclusions These changes in contractile and elastic properties may lead to functional changes of particular interest in sport-related activities as well as in the elderly. Keywords Neuromuscular electrical simulation · Musculo-tendinous stiffness · Maximal angular velocity · Triceps surae · Training
J.-F. Grosset (*) · F. Canon · C. Pérot CNRS UMR 7338, Biomécanique et Bioingénierie, Université de Technologie de Compiègne, 60205 Compiègne cedex, France e-mail: [email protected]
Abbreviations α Torque constant β Angular velocity constant CSA Cross-sectional area Kopt Optimal angular stiffness Kp Passive musculo-articular Stiffness MHC Myosin heavy chain MVC Maximal voluntary contraction NMES Neuromuscular electrical stimulation ′ Θmax Maximal shortening/angular velocity (for in vivo muscle) ′ Optimal shortening/angular velocity Θopt SEC Series elastic component SIMA Musculo-articular stiffness index SIMT Musculo-tendinous stiffness index Topt Optimal torque Vmax Maximal shortening velocity (for isolated muscle) ωopt Optimal angular velocity
J.-F. Grosset UFR Santé Médecine et Biologie Humaine, Université Paris 13, Sorbonne Paris Cité, Bobigny, France
Introduction
D. Lambertz Departemento de Educacao Fisica e Ciencas do Esporte, Universidade Federal de Pernambuco-Centro Academico de Vitoria de Santo Antao, Vitoria de Santo Antao, Brazil
Neuromuscular electrical stimulation (NMES), used as strength training mode, is known to improve neuromuscular function in healthy individuals with an increase in
Communicated by Olivier Seynnes.
13
1404
maximal voluntary contraction (MVC) as the main result. This strength gain could be attributed to neural adaptations as well as muscular changes (see Hortobagyi and Maffiuletti (2011) for review). Furthermore, fibre-type transitions following an NMES training period in sedentary subjects have been reported. More precisely, Perez et al. (2002) reported a decrease in fibres expressing Myosin Heavy Chain (MHC) IIx and I to the profit of fibres expressing MHC IIa. Recently, Gondin et al. (2011) showed an increase in MHC IIa and MHC I in vastus lateralis of sedentary subjects after NMES to the detriment of MHC IIx. It can be assumed that changes in fibre-type proportion due to NMES training would have some mechanical implications. Indeed, the Series Elastic Component (SEC) is composed not only by a passive fraction located at the tendinous level but also by an active fraction located at the cross-bridge level. Thus, a link between fibre-type composition and Series Elastic Component (SEC) characteristics has been proposed (Bosco et al. 1982), slow-twitch motor units eliciting a greater SEC stiffness than fast-twitch ones (Petit et al. 1990). Moreover, in animals different training programmes have shown to induce paired changes in SEC properties and muscle fibres composition (Almeida-Silveira et al. 1994; Goubel and Marini 1987; Pousson et al. 1991). Endurance training induced a decrease in fast-twitch fibre proportion associated with an increase in the stiffness of the series elastic component (SEC) (Goubel and Marini 1987). In contrast, a plyometric training programme leads to an increase in the percentage of fast-twitch fibres associated to a decrease in SEC stiffness (Almeida-Silveira et al. 1994). In humans, Grosset et al. (2009) reported a decrease in SEC stiffness after plyometric training. Regarding the passive part of the SEC, it has not been shown changes in tendon stiffness following plyometric training (Foure et al. 2012; Kubo et al. 2007). Thus, the decrease in SEC stiffness observed after plyometric training is certainly only due to an increase in fast fibre proportion as in animal studies (Simoneau et al. 1985). Following endurance training the increase in SEC stiffness of the ankle plantar flexors (Grosset et al. 2009) is due to an increase in tendon stiffness (Kubo et al. 2001) as well as an increase in slowtwitch fibres as expected from animal studies (Goubel and Marini 1987). Another skeletal muscle adaptive response to changes in fibre-type profile can be evidenced through changes in maximal shortening velocity (Vmax). This characteristic is a function of myosin ATPase and correlation between Vmax and the percentage of fast MHC has been reported (Reiser et al. 1985). Thus, it has been shown that Vmax increased in parallel with an increase in fast-twitch fibre proportion in isolated soleus muscle after stretch–shortening cycle training in rats (Almeida-Silveira et al. 1996). In humans, using isokinetic contractions, Thorstensson et al. (1976) reported
13
Eur J Appl Physiol (2014) 114:1403–1411
correlations between peak torque at the highest speed of muscle shortening and percentage of fast-twitch fibre in knee extensor muscles. Moreover, Lambertz et al. (2001) reported an increase in maximal angular velocity index in plantar flexors after long-term spaceflight and ascribed this change in part to an increase in fast-twitch fibre percentage. To date, skeletal muscle contractile and elastic mechanical properties have never been investigated following highfrequency NMES training period. Thus, the aim of the present study is to quantify musculo-tendinous stiffness as well as maximal angular velocity of triceps surae muscle following a high-frequency NMES training programme. Maximal angular velocity will be assessed using sinusoidal perturbations technique proposed by Desplantez and Goubel (2002).
Methods Subjects The experiment was done on 15 volunteered sedentary college students (age 21.3 ± 0.3 years, stature 177.2 ± 4.3 cm, body mass 70.2 ± 3.4 kg). All the subjects were fully informed about the procedure and gave their informed consent. They were free to withdraw from the study at any time. Each subject was familiarized with the experiment during a preliminary session, one week before starting the pre-training tests. The experimental protocol was approved by the committee of hygiene, safety and ethics at the University of Technology of Compiègne and carried out in accordance with the declaration of Helsinki. All subjects were free from illness or injury. None of the study participants had previously been exposed to NMES or were engaged in systematic resistance training for 12 months or longer prior to taking part in this investigation. NMES training To apply an equivalent training load, based on training sessions number, as compared with previous studies (Gondin et al. 2011; Maffiuletti et al. 2002; Vaz et al. 2013), the subjects completed a 18 sessions of isometric NMES over 4 weeks (i.e. 4–5 sessions per week). Forty-five-induced maximal contractions of the left plantar flexor muscles were induced during each training session (duration ~25 min including warm-up). A standardized warm-up before each session consisted in 5 min of submaximal low-frequency NMES (5 Hz, pulse duration 350 μs). To receive NMES, subjects were comfortably seated with ankle, knee and hip at 90°. Leg and ankle motions were prevented thanks to a custom-made system firmly attached to the floor and positioned on the thigh to ensure standardized isometric
Eur J Appl Physiol (2014) 114:1403–1411
contractions of the plantar flexors throughout the training sessions. A portable stimulator (Compex Sport-P, Medicompex SA, Ecublens, Switzerland) was used to deliver biphasic symmetric rectangular pulses with the following characteristics: frequency 75 Hz, pulse duration 400 μs, 6.25 s on, 20 s off. Three 2-mm-thick self-adhesive electrodes were placed over the left leg. Two positive electrodes (5 × 5 cm) were positioned over the superficial aspect of the left soleus muscle, about 5 cm distal from where the medial and lateral heads of the gastrocnemius muscle join the Achilles tendon. The rectangular (10 × 5 cm) negative electrode was placed along the middorsal line of the leg, and over both medial and lateral gastrocnemius. Current intensity was gradually increased during NMES contractions until the maximally tolerated intensity depending on the subjects’ pain threshold. From one session to another, the maximally tolerated intensity was frequently increased due to subject’s habituation to NMES. The %MVC reached by each subject during NMES training sessions was not monitored in the present study. However, Maffiuletti et al. (2002) reported during a high-frequency NMES training of the triceps surae muscle that the subjects reached between 50 and 70 % MVC during the session. All NMES training sessions were supervised by one of the experimenters. Ergometric device Biomechanical tests were performed using an ankle ergometer (Tognella et al. 1997). The ergometer has two main parts: an electronic device and a mechanical device. The electronic device has a power unit, position and torque transducers and a driving unit equipped with a PC including a 12 bit A/D converter, three timers and a 16TTL output. The mechanical device consists of an actuator (Megatorque motor NSK RS 1010) and transducers: a strain gauge torque (FGP CD 1050) and a 12-bit optical shaft encoder (Hengstler RA 585). Specific menu-driven software controlled all procedures and permitted the simultaneous recording of mechanical signals (torque, angular displacement and angular velocity). A dual-beam oscilloscope gives the subject visual feedback about the procedure in progress. Mechanical tests Each subject sat on an armchair that could be adjusted vertically and horizontally. Dorsal support was provided during the rest periods, but not during voluntary contractions, to prevent extraneous movements and to limit the contribution of other muscles such as the trunk extensor muscles. The left foot was firmly held on to the footplate of the actuator so that the lateral malleolus coincided with the rotation axis of the actuator. The knee was extended to 120°
1405
(180° being full extension) and the ankle was placed at 90° (i.e. neutral position). A maximal voluntary contraction (MVC), corresponding to maximal isometric plantarflexion torque, was developed as fast as possible and maintained for 3 s. This was repeated three times, with 2 min of rest after each trial. The best of the three attempts gave the MVC for the day’s session. To avoid any-time-of-day effect on the investigated parameters, pre- and post-tests were performed at the same time of day (Castaingts et al. 2004; Martin et al. 1999). Elastic properties of the triceps surae musculo-tendinous (MT) complex were assessed by means of the quick-release technique adapted for in vivo experiments (Goubel and Pertuzon 1973). Quick-release movements were achieved around the neutral position by a sudden release of the footplate while the subject maintained a submaximal voluntary isometric torque in plantarflexion. Three attempts were performed at 20, 40, 60 and 80 % MVC, in a random order with 2 min rest between each trial. Then, sinusoidal oscillations (3° peak-to-peak) at different frequencies, ranging from 6 to 16 Hz, were imposed with 1 Hz step to characterize the mechanical properties of the musculo-articular (MA) system, while the subject maintained 20, 40 and 60 % MVC in plantarflexion. Sinusoidal perturbations at rest (i.e. 0 % MVC) were also performed. A 1-min rest interval was given between each trial. Data analysis Quick‑release test Musculo-tendinous stiffness was calculated as the ratio between variations in angular acceleration Θ¨ (as the second derivative of angular displacement, Θ) and angular displacement, multiplied by the corresponding inertia (I) over 20 ms after the sudden release of the footplate. Thus, this formula reads:
¨ S = (∆Θ/∆) ×I
(1)
Then, musculo-tendinous stiffness values were related to the corresponding isometric torque, calculated over the 200 ms that preceded the quick-release movement. The slope of the linear stiffness–torque relationship so obtained was defined as an index of the stiffness of the musculotendinous complex (SIMT). As such, SIMT was proposed to reflect changes in musculo-tendinous stiffness (Lambertz et al. 2001). Sinusoidal perturbations test The data processing for musculo-articular stiffness assessment has been previously reported by Lambertz et al. (2001). The MA elastic properties, including
13
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Eur J Appl Physiol (2014) 114:1403–1411
′ Fig. 1 Maximal angular velocity determination procedure (Θmax ) from sinusoidal perturbation test. In a stiffness–torque (filled square) and viscosity–torque relationships (unfilled circles) and their respective linear fit. Slope and intercept values are used to calculate α
parameter of Hills equation. In b Sinusoidal power–angular frequency (ω) relationship allowing the determination of angular frequency at maximal power (ωopt) used to determine β parameter of Hill’s equation
muscle–tendon and articular structures, were determined under passive (0 % of MVC) and active conditions (20, 40 and 60 % of MVC). Servo-controlled sinusoid length perturbations (3° peak-to-peak whatever the frequency of perturbations ranging from 6 to 16 Hz, see above) were used to establish frequency–response relationships (i.e. Bode diagrams), in which the averaged displacement-to-torque ratios and the phase shifts between displacement and torque were plotted against the imposed frequency. A Bode diagram reflects the mixed mechanical contribution of inertia (I), viscosity (B) and elasticity (K) according to the formula: Z(s) = I.s + B + K.s−1, where Z is the mechanical impedance and s is the Laplace operator. K and B values were calculated at 0, 20, 40 and 60 % MVC to construct the stiffness–torque or viscosity–torque relationships, respectively. Best fit for these relationships was obtained by a linear model: K = k1 T + k2, where T is the torque value, k1 the musculo-articular stiffness index, termed SIMA. k2 is the intercept point (IP). Musculo-articular stiffness in passive conditions was expressed by Kp, the stiffness at 0 % MVC. Finally, B was linearly related to torque to get a slope (b1) and intercept value (b2), as shown in Fig. 1a.
2002). An adaptation of Hill’s equation in terms of angular movements gives the following equation: (T + α) Θ ′ + β = (MVC + α)β (2)
Calculation of maximal angular velocity The hyperbolic relationship between force and velocity observed during isokinetic contraction was used to establish the so-called Hill’s equation [(P + a) (V + b) = (P0 + a)b] (b and a are, respectively, velocity and force constants of Hill’s equation, P is force developed at the shortening velocity V and P0 is tetanic force obtained under isometric condition), allowing assessment of the maximal angular velocity, i.e. the angular velocity at zero force. As in isokinetic condition, it is possible in vivo to evaluate maximal angular velocity at zero torque using sinusoidal perturbations technique (Desplantez and Goubel
13
where α and β are torque and angular velocity constants, respectively, T is torque, and Θ ′ is the angular velocity. Solving this equation when torque is zero allows the calcu′ lation of maximal angular velocity (Θmax ): ′ Θmax = MVC .β/α
(3)
The torque constant (α) can be calculated thanks to equation:
α = b2/b1,
(4)
where b1 and b2 are, respectively, slope and intercept of the viscosity–torque relationship (see Fig. 1a). Finally, the velocity constant (β) is determined with the following equation: ′ β = Θopt Topt + α / MVC − Topt , (5) ′ .is the optimal velocwhere Topt is optimal torque and Θopt ity [i.e. the torque and the velocity at maximal power developed during imposed pulsation (Fig. 1b)]. More details for the method can be found in Desplantez and Goubel (2002). From Eq. (2), the knowledge of α, β and MVC allows the establishment of the individual modelled torque–velocity relationship as well as the calculation of the maximal power (Pmax) and the corresponding torque and angular velocity values.
Statistics SigmaPlot 11.0 (Systat Software, San Jose, CA) was used to run statistical analyses. After a normality test
Eur J Appl Physiol (2014) 114:1403–1411
(Shapiro–Wilk test) validated for each of the investigated parameter, a Student’s t test for paired differences was used to test changes between pre- and post-NMES training protocol in all mechanical parameters (MVC, SIMT, SIMA, ′ Kp and Θmax ) due to NMES, as well as for all calculated ′ parameters necessary for Θmax estimation (Table 2). The level of significance was established at p ≤ 0.05. Values are presented as mean ± SD.
Results Mean maximal intensity applied by the subjects was significantly increased between the first and the fourth week of NMES training period ranging from 31.6 ± 8.7 to 94.1 ± 19.2 mA (p
