Comparison of tensiomyographic contractile properties of the knee muscles between endurance and power athletes

Abstract

BACKGROUND:

Postactivation potentiation (PAP) enhances contractility of skeletal muscle whereas fatigue deteriorates it. Available evidence suggests that the two phenomena may express differently in endurance and power athletes.

OBJECTIVE:

To compare the patterns of change in knee muscle contractility induced by PAP and fatigue between endurance and power athletes.

METHODS:

Eleven endurance and ten power athletes (age: 18–33 years) performed isokinetic fatigue and isometric PAP protocols with knee extensors and flexors on computerised dynamometer. Tensiomyography (TMG) of the vastus medialis and semitendinosus muscle medialis was performed before the protocols and during a 10-min recovery.

RESULTS:

The changes in TMG profile were most pronounced in the vastus medialis of power athletes following the PAP protocol and least pronounced in the semitendinosus of the endurance athletes following the fatigue protocol. The differences between athlete types were most significant for the time-domain TMG parameters of vastus medialis. A significant correlation ( $r=$ 0.51–0.73) between the fatigue indices and changes in TMG parameters was observed for the vastus medialis muscle only.

CONCLUSIONS:

The results show that the TMG patterns of PAP and fatigue in the vastus muscle differ between endurance and power athletes. In this muscle, the changes in TMG parameters are also strongly associated with the degree of fatigue.

Keywords

Tensiomyography skeletal muscle contractility postactivation potentiation peripheral fatigue quadriceps femoris hamstrings

Abbreviations

ANOVA
Analysis of variance
Dm
Muscle displacement
EG
Endurance group
MVIC
Maximal voluntary muscle contraction
MVIC ${}_{N}$
Maximal voluntary muscle contraction normalized to body mass
PAP
Postactivation potentiation
PG
Power group
PP
Peak power
PP ${}_{N}$
Peak power normalized to body mass
PT
Peak torque
PT ${}_{N}$
Peak torque normalized to body mass
QF
Quadriceps femoris
SD
Standard deviation
Tc
Time of contraction
Td
Time of delay
TMG
Tensiomyography
Vc
Velocity of contraction
1. Introduction

Endurance athletes have capacity to produce skeletal muscle contractions at lower force and velocities but are more resistant to fatigue during submaximal motor tasks, whereas power athletes can develop greater muscle force and higher velocities but fatigue more rapidly [1, 2]. These differences in muscle contractility arise from a combination of inherited and acquired neuromuscular characteristics of each individual athlete [2]. The difference in fatigability also exists between muscle groups; the quadriceps femoris (QF) has been shown to be less susceptible to fatigue than the hamstrings [3], mainly due to the difference in muscle fibre content [4]. However, muscle fatigue is not an unambiguous physiological phenomenon. It is preceded with muscle postactivation potentiation (PAP), which occurs immediately after high intensity voluntary muscle contractions [5], but also coexists and possibly counteracts fatigue [6]. The existence of PAP is reflected in a transient and brief increase in rate of torque development after a maximal voluntary muscle contraction [7] that subsides within 5 to 10 minutes [8]. Previous studies suggest that power athletes develop a higher PAP after short series of maximal isometric contractions [9, 10], whereas endurance athletes have a longer lasting PAP after a fatiguing submaximal isometric contraction [11]. PAP has been shown to enhance performance of power athletes [10], whereas its effect in endurance sports is less clear [12].

Accurate assessment of the two physiological phenomena during athletic performance is challenging because of their interaction. Tensiomyography (TMG) has recently gained popularity because it provides a quick and easy assessment of muscle fatigue [13, 14] and does not require voluntary effort from the subject. There is evidence of good to excellent relative reliability and low standard error of measurement for most TMG parameters [15, 16] but lacks more systematic evaluation of diagnostic accuracy and validity for assessment of exercise-induced muscle fatigue [16]. The latter is largely due to the lack of standardization of both TMG measurement and muscle fatigue protocols used in the various studies [13, 14, 17, 18, 19]. A recent meta-analysis found that muscle fatigue induced by acute intense exercise leads to decreases in TMG muscle belly displacement amplitude (Dm), contraction time (Tc), and mean contraction velocity (Vc) [20]. In contrast, the effects of PAP on the TMG profile have not been extensively studied. Beato et al. [21] recently reported that PAP, triggered by an acute series of different exercises with eccentric overload, transiently increased TMG parameters of the QF in the time domain. To our knowledge, no data on contractility of hamstrings have been published to date.

Table 1
Basic subjects’ chracteristics and muscle strength (mean $\pm$ SD) parameters of knee extensors and flexors for mixed gender endurance athlete (EG) and power athlete (PG) groups

	EG ( $n=$ 11)	PG ( $n=$ 11)	$p$ -value
Age (years)	23.4 $\pm$ 5.9	22.1 $\pm$ 3.1	0.545
Body height (cm)	176.3 $\pm$ 7.0	176.3 $\pm$ 11.4	0.999
Body mass (kg)	64.1 $\pm$ 7.2	76.7 $\pm$ 15.7	0.025
Body mass index (kg/m ${}^{2})$	20.6 $\pm$ 1.5	24.4 $\pm$ 2.9	0.001
Quadriceps femoris
MVIC (Nm)	237.2 $\pm$ 46.4	290.0 $\pm$ 42.6	0.032
MVIC ${}_{N}$ (Nm/kg)	3.7 $\pm$ 0.6	3.7 $\pm$ 0.4	0.913
PT 120 ${}^{\circ}$ /s (Nm)	144.8 $\pm$ 30.4	195.9 $\pm$ 55.7	0.015
PT ${}_{N}$ 120 ${}^{\circ}$ /s (Nm/kg)	2.3 $\pm$ 0.4	2.5 $\pm$ 0.3	0.072
PP 120 ${}^{\circ}$ /s (W)	166.4 $\pm$ 32.1	230.2 $\pm$ 76.5	0.020
PP ${}_{N}$ 120 ${}^{\circ}$ /s (W/kg)	2.6 $\pm$ 0.5	2.9 $\pm$ 0.5	0.111
Fatigue index (%)	35.9 $\pm$ 13.7	50.6 $\pm$ 17.8	0.046
Hamstrings
MVIC (Nm)	86.0 $\pm$ 26.6	103.4 $\pm$ 28.1	0.161
MVIC ${}_{N}$ (Nm/kg)	1.3 $\pm$ 0.3	1.3 $\pm$ 0.2	0.925
PT 120 ${}^{\circ}$ /s (Nm)	83.1 $\pm$ 17.1	111.0 $\pm$ 33.9	0.025
PT ${}_{N}$ 120 ${}^{\circ}$ /s (Nm/kg)	1.3 $\pm$ 0.2	1.4 $\pm$ 0.2	0.097
PP 120 ${}^{\circ}$ /s (W)	94.7 $\pm$ 20.0	130.3 $\pm$ 37.8	0.013
PP ${}_{N}$ 120 ${}^{\circ}$ /s (W/kg)	1.5 $\pm$ 0.2	1.7 $\pm$ 0.2	0.040
Fatigue index (%)	26.1 $\pm$ 8.9	29.7 $\pm$ 14.9	0.504

MVIC $=$ maximal volitional isometric contraction torque; PT $=$ peak torque; PP $=$ peak power; ${}_{N}$ $=$ parameter normalized to body mass.

Therefore, the main objective of our study was to determine 1) whether exercise-induced fatigue and PAP of the flexor and extensor muscles of the knee can be differentiated using TMG and 2) whether these responses differ between endurance and power athletes.

2. Materials and methods

2.1 Participants

Twenty-one endurance and power athletes (age 18 to 30 years) took part in the study. Detailed subjects’ characteristics are shown in Table 1. Depending on the type of sport, the subjects were assigned either to the endurance athlete group (EG) or the power athlete group (PG). The EG group comprised four women and seven men ( $N=$ 11) engaged in either long-distance cross-country skiing or long-distance running at least 4 times per week. The PG consisted of three women and seven men ( $N=$ 10) who engaged in either powerlifting, weightlifting or sprint running at least 4 times per week. Inclusion criteria were age of 18–30 years and at least 3 years of participation in a given sport with $\geqslant$ 4 training sessions per week. Exclusion criteria were history of metabolic, pulmonary, hormonal, cardiovascular or neurological disease, radiating lower limb pain or lower limb injury/surgery. To ensure the adequacy of the mixed gender samples, a within-group statistical comparison of the average maximum torques and the normalised maximal torques of males and females was performed.

The study protocol was approved by the National Medical Ethics Committee of the Republic of Slovenia (number: 0120-495/2018/10) and was conducted in accordance with the Declaration of Helsinki. The experiments conducted in this study comply with the current laws of Republic of Slovenia and EU. All subjects received detailed oral and written information and gave their signed informed consent of their voluntarily participation.

2.2 Experimental design

The study was a single-blinded, non-randomized, cross-sectional study comparing TMG responses between two types of athletes (endurance and strength athlete group) induced by two specific exercise protocols (potentiation after activation and fatigue) in two knee muscle groups (extensor and flexor). Subjects participated in two laboratory sessions separated by 48–72 hours. They were instructed to abstain from intense physical activity, caffeine, alcohol, and other substances for at least 24 hours prior to testing. Each subject first performed a warm-up programme consisting of 5-min of stepping at a cadence of 55 steps per minute and low intensity stretching exercises for all major muscle groups of both lower limbs. After a 3-min rest in supine position, resting TMG values were measured in the vastus medialis and semitendinosus muscles of the dominant leg only. The dominance of the leg was defined by dextrality (kicking a ball). The subjects were then taken to a computerized dynamometer where they performed 1) an isometric muscle PAP protocol for the QF and 2) a fatigue protocol for the hamstrings or vice versa; the order of muscle groups and test protocols was counterbalanced between subjects. The second TMG measurement was taken 30-s after completion of each isokinetic protocol and then repeated every minute for 10-min. During the second session, each subject repeated the procedure with the other experimental protocol for each muscle group. The investigator who performed the data analysis did not participate in the laboratory experiments and data collection and was blinded to the group and the exercise protocol during the analysis.

2.3 Position on the dynamometer

The unilateral PAP and fatigue protocols were performed on a computerised dynamometric system (HUMAC NORM, CSMi Medical Solutions, USA). The quadriceps femoris was tested in a seated position with the hip flexed at 85 ${}^{\circ}$ and the axis of knee flexion and extension aligned with the axis of rotation of the dynamometer. The subject’s trunk, pelvis and tested thigh were fixed against the dynamometer chair with rigid straps. The tibia was strapped to the lever of the dynamometer 2 cm above the ankle line, while the other limb was stabilised on a support under the chair. The subject held the arms crossed over the chest. The hamstrings were tested in the prone position with the hip flexed at 10 ${}^{\circ}$ and both knees over the edge of the chair so that the flexion and extension axis of the knee could be aligned with the rotation axis of the dynamometer. The tibia of the tested limb was strapped to the lever of the force gauge 2 cm above the ankle line, while the opposite ankle was manually stabilised against a custom-made support frame by one of the investigators at 30 ${}^{\circ}$ of knee flexion. The subject’s pelvis was secured against the chair with a rigid belt. The subject also held onto the edge of the tilted chair to prevent the trunk from slipping during knee flexion.

2.4 Muscle fatigue protocol

The range of motion of the knee was adjusted from full extension (0 ${}^{\circ}$ ) of the subject to a flexion of 90 ${}^{\circ}$ . The protocol began with a warm-up set consisting of ten repetitions at progressive intensity (50–90% of self-estimated maximal torque). After a 2-min rest, the subject performed 50 consecutive maximal concentric contractions at 120 ${}^{\circ}$ /s with the muscle group tested. The subject received strong verbal encouragement during the exercise. The modified fatigue index of Kawabata and Senda [22] was calculated from the percentage decrease in mean torque (MT) over 50 contractions according to Eq. (1):

$\displaystyle\text{Fatigue index}(\%)=$

(1) $\displaystyle\qquad([\text{MT}_{\text{1 to 3}}-\text{MT}_{\text{48 to 50}}]/% \text{MT}_{\text{1 to 3}})\times 100$

where MT ${}_{\text{1 to 3}}$ represents the MT of the 1 ${}^{\text{st}}$ to 3 ${}^{\text{rd}}$ repetitions and MT ${}_{\text{48 to 50}}$ represents the MT of the 48 ${}^{\text{th}}$ to 50 ${}^{\text{th}}$ repetitions. The highest torque obtained during the protocol was used as peak concentric torque of the tested muscle group.
2.5 Muscle postactivation potentiation protocol

The PAP protocol included isometric contractions performed at 60 ${}^{\circ}$ knee flexion for both extensor (sitting) and flexor (prone lying) muscles. The protocol started with three warm-up contractions with progressive intensity at 25%, 50% and 75% of the self-estimated maximum torque. After a 2-min rest, the subject performed three consecutive 5-s maximal contractions with strong verbal encouragement. The highest torque achieved during the protocol was used as the maximum volitional isometric contraction torque (MVIC) for each subject’s tested muscle group.

2.6 Tensiomyography

The TMG measures mechanical oscillations, thickening, and vibrations of the muscle belly during electrically induced muscle twitches [23]. TMG measurements on the vastus medialis were performed in the supine position with 30 ${}^{\circ}$ of knee flexion (0 ${}^{\circ}$ is extension). Measurements of the semitendinosus were performed in the prone position with 5 ${}^{\circ}$ of knee flexion. Foam pads were used to support the legs and a 2 kg sandbag was placed over the distal tibia to ensure isometric conditions. The vibrations of the muscle belly in response to an electrical twitch were recorded from the skin surface using a sensitive displacement sensor (TMG-S1, Slovenia). The sensor was placed perpendicular to the skin over the muscle belly: for the vastus medialis muscle in the middle of the line between the base of the patella and the innervation point of the muscle [24] and for the semitendinosus muscle in the middle of the line between the medial tibial condyle and the ischial tuberosity. To elicit a muscle twitch, we used a single 1-ms pulse of an electro stimulator (TMG-S1, Slovenia) applied via two adhesive electrodes (5 $\times$ 5 cm, UltraStim X, Axelgaard Manufacturing Co. Ltd., Denmark) 5 cm distal and proximal to the measurement point. The protocol consisted of a series of graded electrical pulses at 10-second intervals, from motor threshold to maximal stimulation, in 5 mA increments. The maximum delay time (Td), contraction time (Tc), amplitude of muscle belly displacement (Dm) and contraction velocity (Vc) were recorded. Dm was defined as the peak amplitude in the path-time curve of the tensiomyographic twitch response. Td was defined as the time between the electrical stimulus and the displacement of the sensor to 10% of Dm. Tc was the time from 10% to 90% of Dm was reached. Vc was calculated according to Eq. (2) [25, 26]:

$\displaystyle\text{Vc}=\text{Dm}_{90\%}/\text{Tc}$ (2)

where Tc is contraction time (ms) between 10% and 90% of peak radial displacement of the muscle belly and Dm ${}_{90\%}$ is the radial displacement (mm) during the period of Tc.

2.7 Sample size estimation

Estimation of minimal sample size at statistical power level of $\geqslant$ 0.90 ( $\beta\leqslant$ 10%) was calculated for interaction effect of factorial ANOVA based on standardized effect size and SD for the differences in Tc and Dm between power and endurance athletes. By assuming that $\geqslant$ 10% difference is of functional relevance, the estimated minimal number of participants was 9.

2.8 Statistical analysis

Figure 1.

Mean (SD) values of (A) delay time (Td), (B) contraction time (Tc), (C) amplitude of muscle belly deformation (Dm) and (D) contraction velocity (Vc) acquired from vastus lateralis muscle with tensiomyography before (rest) and during 10-min recovery following either fatigue (Fatigue, striped symbols) or postactivation potentiation (PAP; closed symbols) exercise protocol for endurance (EG) and power (PG) athlete groups. Red symbols mark difference form rest values at $p<$ 0.05. ${}^{*}$ denotes statistical difference between the groups after fatigue protocol at $p<$ 0.05 and $p<$ 0.01, respectively. # denotes statistical difference between the groups after PAP protocol at $p<$ 0.05 and $p<$ 0.01, respectively. ${}^{\dagger}$ denotes statistical difference between the PAP and fatigue protocol values for EG at $p<$ 0.05. § , §§ and §§§ denote statistical difference between the PAP and fatigue protocol values for PG at $p<$ 0.05, $p<$ 0.01 and $p<$ 0.001, respectively.

Statistical analyses were performed using Statistica software (version 12, StatSoft Inc., Tulsa, Oklahoma, USA). The significance threshold was set at $p<$ 0.05 for all tests. Unless otherwise stated, variables are presented as means $\pm$ standard deviation (SD). Normality of data distribution was analysed using the Shapiro-Wilk test and parametric statistical analysis was considered appropriate. The difference in the means of the anthropometric and muscle strength parameters was tested using Student’s $t$ -test for independent samples. Differences in mean values of TMG parameters were tested using the 3-way (group $\times$ experimental protocol $\times$ time) ANOVA for repeated measures. To reduce number of comparisons, the following seven time-points were used: rest (pre-exercise) and 30-s, 60-s, 3-min, 6-min and 10-min postexercise. The statistics reported for the interaction of the factors are the p-value ( $\alpha$ ), F-value, effective size ( $\eta p^{2}$ ) and statistical power (1 $-$ $\beta$ ). In case of significant interaction, the post hoc pairwise comparisons were made with Tukey’s honestly significant difference test. To assess association between FI and changes ( $\Delta{p}$ ) in TMG parameters ( $\Delta$ Td, $\Delta$ Tc, $\Delta$ Dm and $\Delta$ Vc) at 30 s after cessation of exercise, univariate linear regressions were performed on the pooled data of both athletes’ groups. Pearson’s correlation coefficient ( $r$ ), coefficient of determination ( $r^{2})$ was calculated and reported.

3. Results

The basic comparison between male and female subjects in EG showed no significant differences ( $p=$ 0.092–0.939) in maximal muscle strength of QF (males: MVIC $=$ 252.3 $\pm$ 53.3 Nm, MVIC ${}_{N}$ $=$ 3.6 $\pm$ 0.7 Nm/kg, PT 120 ${}^{\circ}$ /s $=$ 160.5 $\pm$ 31.0 Nm; PT ${}_{N}$ 120 ${}^{\circ}$ /s $=$ 2.3 $\pm$ 0.4 Nm/kg; vs. females: MVIC $=$ 205.0 $\pm$ 11.0 Nm, MVIC ${}_{N}$ $=$ 3.6 $\pm$ 0.6 Nm/kg, PT 120 ${}^{\circ}$ /s $=$ 121.5 $\pm$ 16.0 Nm; PT ${}_{N}$ 120 ${}^{\circ}$ /s $=$ 2.1 $\pm$ 0.4 Nm/kg) and the hamstrings (males: MVIC $=$ 95.0 $\pm$ 30.5 Nm, MVIC ${}_{N}$ $=$ 1.4 $\pm$ 0.4 Nm/kg, PT 120 ${}^{\circ}$ /s $=$ 94.2 $\pm$ 14.4 Nm; PT ${}_{N}$ 120 ${}^{\circ}$ /s $=$ 1.4 $\pm$ 0.2 Nm/kg; vs. females: MVIC $=$ 67.5 $\pm$ 7.8 Nm, MVIC ${}_{N}$ $=$ 1.2 $\pm$ 0.1 Nm/kg, PT 120 ${}^{\circ}$ /s $=$ 66.3 $\pm$ 3.1 Nm; PT ${}_{N}$ 120 ${}^{\circ}$ /s $=$ 1.2 $\pm$ 0.1 Nm/kg). Likewise, the comparison between male and female subjects in PG showed no significant differences ( $p=$ 0.137–0.746) in maximal muscle strength of QF (males: MVIC $=$ 311.0 $\pm$ 90.7 Nm, MVIC ${}_{N}$ $=$ 3.9 $\pm$ 0.4 Nm/kg, PT 120 ${}^{\circ}$ /s $=$ 204.7 $\pm$ 62.0 Nm; PT ${}_{N}$ 120 ${}^{\circ}$ /s $=$ 2.5 $\pm$ 0.3 Nm/kg; vs. females: MVIC $=$ 241.0 $\pm$ 29.5 Nm, MVIC ${}_{N}$ $=$ 3.4 $\pm$ 0.2 Nm/kg, PT 120 ${}^{\circ}$ /s $=$ 175.3 $\pm$ 39.0 Nm; PT ${}_{N}$ 120 ${}^{\circ}$ /s $=$ 2.5 $\pm$ 0.2 Nm/kg) and the hamstrings (males: MVIC $=$ 110.1 $\pm$ 26.2 Nm, MVIC ${}_{N}$ $=$ 1.4 $\pm$ 0.2 Nm/kg, PT 120 ${}^{\circ}$ /s $=$ 117.7 $\pm$ 34.1 Nm; PT ${}_{N}$ 120 ${}^{\circ}$ /s $=$ 1.5 $\pm$ 0.1 Nm/kg; vs. females: MVIC $=$ 87.7 $\pm$ 31.0 Nm, MVIC ${}_{N}$ $=$ 1.2 $\pm$ 0.3 Nm/kg, PT 120 ${}^{\circ}$ /s $=$ 95.3 $\pm$ 33.8 Nm; PT ${}_{N}$ 120 ${}^{\circ}$ /s $=$ 1.3 $\pm$ 0.3 Nm/kg).

Figure 2.

Mean (SD) values of (A) delay time (Td), (B) contraction time (Tc), (C) amplitude of muscle belly deformation (Dm) and (D) contraction velocity (Vc) acquired in semitendinosus muscle with tensiomyography before (rest) and during 10-min recovery following either fatigue (Fatigue, striped symbols) or postactivation potentiation (PAP; closed symbols) exercise protocol for endurance (EG) and power (PG) athlete groups. Red symbols mark difference form rest values at $p<$ 0.05. ${}^{*}$ and ${}^{**}$ denote statistical difference between the groups after fatigue protocol at $p<$ 0.05 and $p<$ 0.01, respectively. # and ## denote statistical difference between the groups after PAP protocol at $p<$ 0.05 and $p<$ 0.01, respectively. ${}^{\dagger}$ denotes statistical difference between the PAP and fatigue protocol values for EG at $p<$ 0.05. § and §§ denote statistical difference between the PAP and fatigue protocol values for PG at $p<$ 0.05 and $p<$ 0.01 respectively.

A comparison of age, anthropometric characteristics and muscle strength parameters between mixed gender athlete groups is summarised in Table 1. There were no significant differences in age and height between the groups, whereas body mass and body mass index ( $p<$ 0.05) were 19.7% and 17.9% higher in PG, respectively. Subjects from PG had 22.3% higher ( $p=$ 0.032) MVIC torque, 35.3% higher ( $p=$ 0.015) peak isokinetic torque and 38.3% higher ( $p=$ 0.020) peak QF muscle power. Similarly, subjects from PG had 33.6% higher ( $p=$ 0.025) peak isokinetic torque, 37.6% higher ( $p=$ 0.013) peak power and 13.3% higher ( $p=$ 0.040) peak power of the hamstrings normalised to body mass. EG had a 14.7% lower ( $p=$ 0.046) fatigue index of the QF muscle, while no significant difference in fatigue index was found between the groups for the hamstrings.

3.1 Tensiomyography

Figure 3.

Univariate linear regressions and correlation coefficients between fatigue index of vastus medialis (VM) muscle obtained from 50-repetition isokinetic fatigue protocol at 120 ${}^{\circ}$ /s and changes ( $\Delta)$ in (A) delay time ( $\Delta$ Td), (B) contraction time ( $\Delta$ Tc), (C) amplitude of muscle belly lateral deformation ( $\Delta$ Dm) and (D) velocity of contraction ( $\Delta$ Vc) acquired with tensiomyography 30 s after the test.

The most significant changes in TMG parameters were observed in both knee muscles within the first 60-s of recovery after both fatigue and PAP protocol; in some cases, they were still present 10-min after exercise (Figs 1 and 2).

In the vastus medialis muscle, a significant interaction of all factors was observed for Td ( $p=$ 0.006, $F=$ 3.53, $\eta p^{2}=$ 0.157, $1-\beta=$ 0.904), Tc ( $p=$ 0.003, $F=$ 3.93, $\eta p^{2}=$ 0.171, $1-\beta=$ 0.935) and Vc ( $p=$ 0.033, $F=$ 2.54, $\eta p^{2}=$ 0.118, $1-\beta=$ 0.768), whereas for Dm a significant interaction of protocol $\times$ time was noted ( $p<$ 0.001, $F=$ 20.64, $\eta p^{2}=$ 0.521, $1-\beta=$ 1.000). A pairwise comparison between protocols showed that Td, Tc and Vc were shorter in both EG ( $p<$ 0.05) and PG ( $p<$ 0.001), while Dm was higher only in PG ( $p<$ 0.01), after the PAP protocol. A pairwise comparison between groups showed that Td and Tc were 5% and 10% longer ( $p<$ 0.05) in PG during first 60-s of recovery after the fatigue protocol, respectively. In contrast, Dm and Vc were 73% and 67% lower ( $p<$ 0.05) in the EG already during rest and also at 30-s and 60-s of recovery after the fatigue protocol, respectively, but were not significantly different afterwards. The differences between groups after the PAP protocol were not significant (Fig. 1).

In the semitendinosus muscle, the interaction of all three factors was not significant for any of the TMG parameters. A significant interaction of protocol $\times$ time was noted for Td ( $p<$ 0.001, $F=$ 22.934, $\eta p^{2}=$ 0.547, $1-\beta=$ 1.000), Tc ( $p<$ 0.001, $F=$ 5.39, $\eta p^{2}=$ 0.230, $1-\beta=$ 0.986) and Vc ( $p<$ 0.001, $F=$ 10.96, $\eta p^{2}=$ 0.378, $1-\beta=$ 0.999), but was non-significant for Dm ( $p=$ 0.965, $F=$ 0.19, $\eta p^{2}=$ 0.011, $1-\beta=$ 0.093). A pairwise comparison between protocols showed shorter Td in both EG ( $p<$ 0.05) and PG ( $p<$ 0.01), while Tc was shorter ( $p<$ 0.05) and Vc was higher ( $p<$ 0.05) in PG only, following the PAP protocol. A pairwise comparison between the groups showed no significant difference for Td and Tc. In contrast, Dm was consistently $\sim$ 62% higher ( $p<$ 0.01) in EG at all time points. Similarly, Vc was $\sim$ 45% higher ( $p<$ 0.01) in the EG group at rest and again at 6-min and 10-min of recovery following both exercise protocols (Fig. 2).

3.2 Relationship between tensiomyography and fatigue indices

Figure 4.

Univariate linear regressions and correlation coefficients between fatigue index of semitendinosus (ST) muscle obtained from 50-repetition isokinetic fatigue protocol at 120 ${}^{\circ}$ /s and changes ( $\Delta)$ in (A) delay time ( $\Delta$ Td), (B) contraction time ( $\Delta$ Tc), (C) amplitude of muscle belly lateral deformation ( $\Delta$ Dm) and (D) velocity of contraction ( $\Delta$ Vc) acquired with tensiomyography 30 s.

The results of the linear regression and correlation analysis between FI and the TMG parameters recorded at 30-s of recovery after the fatigue test are shown in Figs 3 and 4. For the vastus medialis, a high positive correlation was found with $\Delta$ Td ( $r=$ 0.727; $p<$ 0.001), a moderate positive correlation with $\Delta$ Tc ( $r=$ 0.609; $p=$ 0.003) and a moderate negative correlation with both $\Delta$ Dm ( $r=$ -0.508; $p=$ 0.019) and $\Delta$ Vc ( $r=$ -0.603; $p=$ 0.004) (Fig. 3). For the semitendinosus, all correlations between FI and TMG parameters were low and non-significant (Fig. 4).

4. Discussion

This is the first study of PAP and fatigue profiles of knee muscle contractile properties of power and endurance athletes assessed by TMG. In general, changes in TMG parameters were most pronounced in power athletes following the PAP protocol and least pronounced in endurance athletes following the fatigue protocol. The differences between the groups were the highest and most significant for the time-domain TMG parameters of vastus medialis during the 10-min recovery after the fatigue protocol, whereas no significant differences in the response to either type of exercise were detected for the semitendinosus muscle.

The significantly higher isometric and isokinetic peak torque and power of PG confirmed our assumption of initial differences in knee muscle contractile capacity between power and endurance athletes. Considering that power athletes had $\sim$ 20% more body mass than endurance athletes, while they had similar ( $p>$ 0.90) MVIC ${}_{N}$ torques of both the QF and hamstrings, the difference in strength can largely be attributed to the difference in muscle mass between the groups (Table 1).

4.1 The effects of postactivation potentiation on TMG profile

The influence of PAP on TMG parameters has not been extensively studied yet, so there is little published data. This is partly because it is experimentally difficult to separate PAP from fatigue, as the two phenomena are interrelated and overlapping [6]. Beato et al. [21] recently reported that different types of exercises with eccentric overload enhance the PAP response of all three superficial QF muscle heads in an exercise-specific manner. As their time frame for TMG acquisition was substantially different from ours, a direct comparison of the findings is difficult. In general, they observed a 5–16% decrease in Dm, Tc, Td and Vc in the vastus medialis and rectus femoris 4 min after completion of exercise [21]. In contrast, the maximal modulation of TMG parameters of our subjects was observed as early as 30-s after PAP protocol and subsided rapidly thereafter. Of note, the observed pattern of change in TMG parameters was also markedly different between the two muscles. In the vastus medialis, Td and Tc were decreased by 5–7% and 15–19%, respectively, and Vc was increased in both athlete groups (30–44%), while Dm was increased only in the PG group (17%). The pattern of TMG changes in the semitendinosus muscle was even more consistent across the athlete groups and showing a non-significant trend of less pronounced changes in endurance athletes (Fig. 2). That the PAP induced by maximal isometric contractions is lower in endurance athletes than power athletes has been demonstrated previously using the interpolated supramaximal muscle twitch technique in both men [9, 11] and women [10]. Interestingly, these studies showed differences between types of athletes for the QF muscle, whereas in our study the differences, albeit not significant, were only observed for the semitendinosus muscle. The rational for contradictory findings between studies may arise from different measurement methods used for assessment of contractility. The maximal muscle twitch is elicited by stimulation of the femoral nerve and hence activates the entire QF simultaneously, whereas TMG measurement is limited to an isolated muscle head twitch. It might thus be that other three QF heads are more susceptible to PAP than the vastus medialis. This needs to be investigated further.

The decrease in Tc, Td and increase in Vc observed with PAP all indicate increased muscle reactivity and contractility. The increase in Vc with PAP is physiologically sounder than the decrease in Vc observed by Beato et al. [21], as the speed of muscle contraction should be increased by potentiation and not suppressed, which has been demonstrated also by Garcia-Manso et al. [17] for biceps brachii.

Our results thus confirm the paradigm that a short PAP protocol consisting of near-maximal isometric contractions elicits an immediate but short-lasting PAP response in both types of athletes, so it must be performed as close as possible to the sporting event to use its full potential for enhancing performance [27].

4.2 The effects of muscle fatigue on TMG profile

Our results show that the degree of exercise-induced local fatigue in the QF muscle differed significantly between endurance and power athletes (fatigue index 35.9% in EG vs. 50.6% in PG), while it was lower in the hamstrings and did not differ significantly between groups (26.1% in EG vs. 29.7% in PG). The difference in the degree of muscle fatigue between the athlete groups was clearly reflected in the modulation of TMG parameters during the 10-minute recovery period (Figs 1 and 2). Furthermore, fatigue was more pronounced in the vastus medialis muscle than in the semitendinosus muscle. The TMG profile of the fatigued vastus medialis was similar to that reported by other authors for different QF muscle heads. The 34% decrease in Dm observed in our power athletes was comparable to the decrease in Dm observed in the rectus femoris muscle fatigued either by high intensity cycloergometry to exhaustion (42%) [28] or by various types of resistance exercise (25%) [29], whereas a slightly smaller decrease in Dm of various QF heads (18–22%) was observed after sustained submaximal isometric contraction to failure [18]. A similar decrease in Dm was also observed in the biceps brachii fatigued by either high-intensity (21%) or high-volume (17%) resistance exercise [17], and in the gastrocnemius muscle fatigued by low-frequency electrical stimulation (17%) [26]. Considering that decreased Dm is associated with increased stiffness of the muscle-tendon complex [30, 31], it appears that muscle tone is increased during peripheral muscle fatigue. This could be due to increased phosphorylation of the myosin light chains, but also to changes in the viscoelastic properties of the muscle connective tissue. In contrast to Dm, the changes in Tc with fatigue were less pronounced; a slight decrease was observed in both groups of athletes from about 3-min after recovery (Fig. 1b). As the validity of Tc for assessing the speed of muscle contraction is influenced by concomitant changes in Dm, the calculation of Vc has been proposed as a more reliable index [25, 26]. Although it is reasonable to assume a decrease in Vc with fatigue, the evidence from the literature is inconclusive. The 41% decrease in Vc of the medial vastus observed in our subjects confirms the findings of other authors who reported a 10–25% decrease in Vc with QF fatigue [13, 29]. In contrast, García-Manso et al. [17] reported an increase in Vc of approximately 20% during repeated sets of resistance exercise. It can be argued that the increase in Vc is a sign of muscle PAP rather than fatigue. That fatigue was characterised by a decrease in Dm and Vc with a concomitant increase in Td and Tc is also evident from the moderate to high positive correlation between the fatigue index and Td and Tc and the negative correlation with Dm and Vc (Fig. 3). These results are consistent with previous reports of a positive correlation between the decrease in maximal isometric strength and the decrease in Dm and Vc [29, 32]. Why the correlations between FI and TMG parameters were only marginal and nonsignificant for the semitendinosus muscle is unclear and needs further investigation. At least partly, this can be due to somewhat narrower range of fatigue indices developed in semitendinosus (12–52%) compared to vastus medialis (10–76%), which reduces sensitivity of association analysis for semitendinosus.

When comparing different types of athletes, De Paula Simola et al. [13] reported a 20% decrease in Dm of QF in power athletes after 6 days of intensive strength training, but only an 11% decrease in endurance athletes. The change is consistent with our results, but in a substantially different time frame; they measured TMG 12–72 hours after the last training session [13], whereas in the present study the majority of TMG parameters returned to baseline values within 10-min of training. The differences in the temporal profile of TMG suggest that repeated daily exercise with intense training produces longer-lasting changes in muscle contractility than a single high-intensity exercise. The difference in TMG profile between endurance and power athletes following the fatigue protocol can be attributed to differences in their ability to co-host both physiological phenomena. As Morana and Perrey [11] have shown, the increased resistance to fatigue in endurance athletes allows a longer predominance of PAP over fatigue, whereas in power athletes PAP is overridden by fatigue much earlier ( $<$ 2 min).

By using external electrical muscle twitches, TMG primarily measures peripheral fatigue at the skeletal muscle level [13, 14]. Because TMG does not directly assess the physiological mechanisms of muscle fatigue, we can only speculate about possible mechanisms of the changes in TMG profile that occurred with fatigue in our subjects. At the cellular level, initial muscle fatigue is characterised by reduced efficiency of excitation-contraction coupling, which then leads to impaired membrane conductance and, in more severe cases, may even lead to cell destruction [33]. Hunter et al. [32] found that sustained muscle fatigue observed several days after intense eccentric exercises of the elbow flexors was characterised by a decrease in Dm and an increase in Tc, coinciding with the development of intense delayed-onset muscle soreness. Therefore, they hypothesised that exercise-induced muscle damage is a key factor in modulating the TMG profile [32]. This was less likely in our subjects because they performed a fatigue protocol with concentric contractions and the TMG profile was only measured within a short period after the end of the protocol, when no pain was present. However, as the extent of muscle microinjury was not investigated in our subjects, no definitive conclusion can be drawn about the possible influence of muscle microinjury on the TMG profile. Further research is needed in this regard.

4.3 The differences in fatigability of knee extensors and flexors

Our results show distinct differences between the muscle groups in their response to the two experimental protocols. Different TMG patterns of knee muscle groups were also reported after an Ironman triathlon [14] and during the season in road cyclists [30]. There are several factors that may have contributed to the fundamentally different patterns of change in muscle strength and TMG parameters in knee extensors and flexors. Muscle composition is thought to be an important factor in the differential fatigability of each muscle group [34]. The QF muscle has been shown to be less susceptible to fatigue than the hamstrings [3, 22], largely due to the different proportion of type I and type II muscle fibres [4]. In addition, differences in the composition of the muscle fibre types of the vastus lateralis have been observed between endurance runners, power athletes and strength-trained individuals [35]. While the QF is a complex, multi-head muscle, which largest part (i.e. the vastii) contains a smaller proportion of II type fibres (32–47%) [36], the hamstrings contain a predominant proportion of II type fibres ( $\sim$ 58%), of which the biceps femoris contains 48–59%, the semitendinosus 50–69% and the semimembranosus 44–55% [37]. However, the ratio of muscle fibre types in the hamstrings remains unclear to date. Biceps femoris of young and middle-aged men has been reported also to have a balance of both fibre types (50/50%) [38, 39], hence challenging the common paradigm that hamstrings are predominantly fast, glycolytic muscles. Furthermore, the composition of fibre types in hamstrings has been shown to have little relationship with maximal strength or explosive power [39]. Our results showed that isokinetic torque of hamstrings was less susceptible to fatigue than that of QF. In addition, all Vc values of semitendinosus (group pooled data for resting Vc $=$ 154 $\pm$ 57 mm/s) were substantially lower than of vastus medialis (group pooled data for resting Vc $=$ 275 $\pm$ 65 mm/s), clearly suggesting that hamstrings are not predominantly fast glycolytic muscle group.

Overall, our results support the findings of a recent meta-analysis that muscle fatigue induced by repeated high-intensity resistance exercise protocols leads to a decrease in muscle tone (increase in Dm), a shorter contraction time (Tc) and a lower contraction velocity (Vc) [20]. This counteracts the TMG results from studies of longer-lasting type of fatigue induced by less intense but more chronic repetitive muscle contractions (i.e. marathon running, etc.), where reduction in muscle tone was found [14, 40].

4.4 Methodological limitations

The main methodological limitation of our study is that we have no histological evidence of the actual distribution of muscle fibre types in our subjects, so we can only assume that they had a substantially different muscle composition. However, based on their athletic history and the differences in body mass, muscle peak torque and power, and fatigue index, it is very likely that the average composition of the vastus medialis muscle was significantly different between the two groups of athletes. This cannot be said with the same degree of certainty for the semitendinosus muscle and requires further investigation on larger samples with muscle biopsies. Some differences between genders, e.g. the higher percentage of IIx fibers expected for males, may have interfered with group comparison as an additional female subject was recruited in EG. In addition, somewhat different muscle training adaptations of sprinters and powerlifters may have reduced a homogeneity of PG and hence diminished observed differences between the groups of athletes. This should be accounted for in subjects’ inclusion criteria of future studies.

5. Conclusions

The results show that the TMG profiles of postactivation potentiation and fatigue in the vastus medialis differ between endurance and power athletes, but less so in the semitendinosus. In general, the changes in TMG parameters induced by the two experimental protocols were of short duration and peaked within the first minute after exercise. The changes in TMG profile were most pronounced in the vastus medialis of power athletes following the PAP protocol and least pronounced in the semitendinosus of the endurance athletes following the fatigue protocol. Furthermore, changes in TMG parameters were strongly associated with the degree of fatigue only in the vastus medialis muscle. The observed differences in the TMG profiles of endurance and power athletes suggest that their knee muscles differ in their ability to express postactivation potentiation and fatigue resistance.

Author contributions

CONCEPTION: Alan Kacin and Matej Ipavec.

PERFORMANCE OF WORK: Matej Ipavec and Žiga Kukec.

INTERPRETATION OR ANALYSIS OF DATA: Alan Kacin and Matej Ipavec.

PREPARATION OF THE MANUSCRIPT: Matej Ipavec and Alan Kacin.

REVISION FOR IMPORTANT INTELLECTUAL CONTENT: Alan Kacin, Matej Ipavec and Žiga Kukec.

SUPERVISION: Alan Kacin.

All authors read and approved the final version of the manuscript.

Ethical considerations

Funding

This research was financially supported by Javna agencija za raziskovalno dejavnost Republike Slovenije under Grant P3-0043 and Univerzitetni klinični center Ljubljana under Grant 20190041 and Grant 20200063.

Footnotes

Acknowledgments

The authors are indebted to all the volunteers who participated in the study.

Conflict of interest

The authors declare that they have no competing interest or conflicts of interest connected to this study. None of the authors have any financial or personal relationships that could inappropriately influence this work.

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Comparison of tensiomyographic contractile properties of the knee muscles between endurance and power athletes

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

Abbreviations

Table 1 Basic subjects’ chracteristics and muscle strength (mean ± SD) parameters of knee extensors and flexors for mixed gender endurance athlete (EG) and power athlete (PG) groups

2.1 Participants

2.2 Experimental design

2.3 Position on the dynamometer

2.4 Muscle fatigue protocol

2.6 Tensiomyography

2.8 Statistical analysis

4.1 The effects of postactivation potentiation on TMG profile

4.2 The effects of muscle fatigue on TMG profile

4.3 The differences in fatigability of knee extensors and flexors

4.4 Methodological limitations

5. Conclusions

Author contributions

Ethical considerations

Funding

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Basic subjects’ chracteristics and muscle strength (mean $\pm$ SD) parameters of knee extensors and flexors for mixed gender endurance athlete (EG) and power athlete (PG) groups