Dry BMs are least invasive and thus usually the ones most easily determined. Dry BMs include measurement of muscle force (power output) before and after or during a workload, analysis of electrophysiological recordings, assessment of cardiac parameters, and scales or questionnaires.
Power output
There are various test assemblies to perform exercise and to assess power output from this workload to determine muscle fatigue.
Direct measurement of muscle force. Measuring muscle force before and after predefined workload is one of the most frequently applied means to measure EIMUF. Loss of power output during exercise may reflect muscle fatigue. Muscle force before and after a given task can be measured in a single muscle, in a group of muscles, or in all muscles. Measuring muscle force may be carried out with dynamometers, power output measuring devices (probes), clinical assessment of muscle force, or more globally with questionnaires. Various power output measuring devices are available. Various types of exercise may precede force measurement [
3]. Leg and arm force production is reduced after any exercise but particularly after a marathon [
14]. Maximum isometric force-generating capacity (MIFGC) is reduced immediately after eccentric contraction [
38]. MIFGC remains depressed 48 h after exercise [
38]. External/internal rotation isokinetic torque [
39] is reduced after exercise, Power output is also reduced after fatiguing leg press exercise [
40]. In this test, power is calculated as the instantaneous product of displacement velocity and applied force, whereas work output is calculated as vertical displacement of the weight plates times applied force [
40]. Even peak power, however, may show diurnal fluctuations with higher values in the evening compared to the morning [
21]. Force of bulbar muscles in children can be assessed by means of the slurp test [
41].
Tongue pressure. An example of assessing power output of bulbar muscles is by measuring the tongue pressure. In neuromuscular disorders with bulbar involvement, such as myasthenia, amyotrophic lateral sclerosis (ALS), bulbo-spinal muscular atrophy (SBMA), oculopharyngeal muscular dystrophy (OPMD), myotonic dystrophy type 1 (MD1), or mitochondrial disorders (MIDs), assessment of bulbar functions is mandatory. In a study of 47 patients with SBMA tongue pressure was measured by means of an intra-aortic pressure probe and questionnaires which assessed swallowing [
42]. Tongue pressure was reduced in SBMA patients within 3y after disease onset. Tongue pressure was reduced even in patients without dysphagia and repetition of swallowing compensated for tongue weakness in these patients [
42]. Tongue pressure was positively correlated with bulbar-related functional scales [
42]. Tongue pressure more strongly correlated with muscle strength of the pharyngeal, neck, and upper limb muscles than with lower limb muscles. Though tongue pressure is not validated as a BM of focal EIMUF, it appears a promising monitor of focal EIMUF and weakness of bulbar muscles since power output can be measured over time before and after exercise and correlates well with scales assessing swallowing [
42].
Jumping. A further possibility to assess the power output is by means of jumping tests. Most frequently applied is the CMJ test which collects and analysis parameters such as mean power, peak velocity, peak force (PF), peak power (PP), peak torque, jump height, flight time, contact time, and rate of force development (RFD) [
3,
43,
44]. The test induces only a minimal amount of additional fatigue itself and thus is useful to monitor EIMUF when carried out before and after exercise [
3,
45]. After an isokinetic, concentric exercise peak torque and RFD decreased even 24 h after exercise [
43]. Jumping performance seems to deteriorate for as long as 72 h post-exercise whereas strength remains unchanged after an acute bout of intense polymetric exercise [
46]. Other jumping tests for measuring the power output include the static jump (SJ) test [
46], the vertical jump test [
47], and the drop jump [
47].
Cycling. Another possibility to assess the power output is by means of cycling on an ergometer. Most commonly applied is the cycle ergometer sprint test which specifically quantifies the concentric component of the fatigue-induced decrement of force production in muscle, which may be overlooked by the CMJ test [
48]. The cycle ergometer sprint test is a method of monitoring EIMUF in endurance or power-team-sport athletes [
48].
Walking. Walking test represent a frequently applied means to assess the power output. Examples of walking tests are the 6 m walking test, the 400 m walking speed test, the timed-up-and-go test [
49], the 12-min self-paced walking test, and stair climbing [
49].
Running. Another possibility to assess the power output is by measuring running speed or distance. Reduction of running speed is a simple means of indirectly measuring EIMUF but only a global parameter since assessment may also include central fatigue. Decrease of running speed can be particularly observed in long-distance runners (marathoners) [
14]. In a study of 22 endurance athletes carrying out the UMTT, the maximum running speed test remained unchanged after the UMTT, possibly due to PAP [
36]. Other running tests include the maximum running speed over a distance of 20 m (20 m sprint test) [
36,
47], the total high-intensity running distance (THIR) [
45], and the repeated sprint ability (RSA) exercise [
50]. Most of the power output tests show diurnal fluctuations with higher values in the afternoon compared to the morning [
50].
Electrophysiological BMs
Surface EMG analysis. Applying surface-EMG, an interference pattern is recorded by bipolar surface electrodes positioned over the endplate zone of the muscle of interest [
51]. Signals are then passed to an A/D converter, are band-pass filtered, and converted to root mean square (RMS) or mean rectified voltage for EMG amplitude, which is roughly equivalent to the mean rectified value (MRV). Additionally, surface EMG interference patterns may be analysed by fast Fourier transformation for median frequency, mean power output, or mean frequency (MF) over a distinct epoch [
8,
52]. In a study of 12 healthy males performing standardised exercise with two different loadings on a knee extension device, post-loading EMG-amplitude was either reduced or increased depending on the type of loading [
8]. MRV or RMS are typically increased after exercise. MF and mean power output are typically reduced after exercise [
8]. Muscle fatigue is thus characterised by an increase in the EMG interference-pattern amplitude (recruitment of additional motor units, increase in firing frequency, synchronisation of discharges) and a shift of the spectrum to the left [
53,
54]. Recovery from muscle fatigue is characterised by a decrease of the EMG-amplitude and a shift of the spectrum to the right [
53].
Muscle torque. To assess muscle torque, muscle stimulation is performed on the resting muscle via self-adhesive surface electrodes by delivering single rectangular pulses by a constant-current stimulator to the supplying nerve until a torque plateau is observed [
8]. Antagonist muscles are not stimulated. The parameters of interest include the maximum isometric torque, the maximum twitch torque (peak torque), and the half-relaxation time [
8]. After exercise the peak torque is typically reduced using variable resistance loadings [
8]. Reduction of maximum twitch torque is more pronounced in young as compared to old subjects [
8].
M-wave duration. A further electrophysiological method to monitor EIMUF is the assessment of the M-wave after stimulation of motor nerves. Stimulation electrodes (cathodes) are placed such that a weak stimulation current gives the strongest response [
8]. Then the stimulating current is increased in 10 mA steps until a clear plateau in the M-wave amplitude is reached. Thereafter an additional 25 % of stimulation current is applied (supramaximal stimulation) [
8]. In a study of 12 healthy males performing standardised exercise on a knee extension device, post-loading peak-to-peak M-wave duration was significantly increased while area and amplitude were decreased after the bout [
8].
Conduction velocity. In some studies EIMUF resulted in reduction of the nerve conduction velocity, irrespective if the proband carried out eccentric or concentric exercise [
55]. In power athletes as well as in endurance athletes the degree of EIMUF correlated negatively with the nerve conduction velocity [
52]. Other studies, however, did not confirm these findings [
56]. Contrary to nerve conduction velocity, muscle fiber conduction velocity (MFCV) as assessed by surface EMG decreased with EIMUF at least during dynamic exercise [
23,
57,
58]. During static exercise by means of fatiguing isometric contractions, on the contrary, MFCV remained unchanged [
58].
Transcranial magnetic stimulation (TMS). In 8 patients with electrical injury undergoing a 2 min exercise with MVC, TMS revealed prolongation of the silent period and an increase of the area and amplitude of the M-wave response [
59]. These effects could be increased if patients were exposed to muscle ischemia induced by a blood pressure cuff to simulate EIMUF [
59]. The technique allows differentiation between the central and peripheral contribution to EIMUF [
59].
EMG fatigue threshold. The EMG fatigue threshold is defined as the exercise intensity an individual can maintain indefinitely without the need to recruit additional motor units, which is associated with an increase in the amplitude of the interference pattern [
60]. Recently, a new practical and reliable method to determine the EMG fatigue threshold has been introduced [
60]. The physical working capacity at fatigue threshold (PWCFT) is defined as average of the highest power output that results in a non-significant slope coefficient for the EMG amplitude vs. time relationship and the lowest power output that results in a significant positive slope coefficient [
61]. Short term exercise increases the fatigue threshold [
62]. By means of the PWCFT heavy from severe domains of exercise intensity can be differentiated [
63]. Helpful in this respect are also the power output associated with the gas exchange threshold (PGET), the respiratory compensation point (PRCP), and the critical power [
64,
65]. Usually, aerobic exercise training at PWCFT is carried out as a task to produce EIMUF [
66]. The absent correlation between PWCFT, PGET, and MPFFT suggests that different physiological mechanisms underlie these three fatigue thresholds [
65].
Cardiac parameters. EIMUF is dependent on the muscular blood flow and thus on cardiac function, therefore monitoring and evaluation of basic cardiac parameters can be helpful for assessing EIMUF. Frequently applied cardiac parameters include the heart rate, the post-exercise heart-rate recovery (HRR, rate at which heart rate declines after exercise) [
3,
45], and the heart rate variability (LnrMSSD) calculated from the long-term ECG [
3,
45]. Heart rate is one of the most common parameters to assess the internal load during exercise [
3]. This is because of the linear relationship between heart rate and oxygen consumption during steady state exercise [
3]. Since there is a positive correlation between THIR, rating of perceived fatigue, and CMJ, HRR and LnrMSSD are promising candidates for non-invasive BMs of the fatigue status in elite soccer players [
45].
Movement kinematics and kinetics. Parameters of movement kinematics or kinetics correlated with changes in the muscle fatigue state as measured by EMG interference pattern [
67,
68]. Knee and ankle kinematics can be recorded via optical motion capture [
11,
69]. For example, kinematics and kinetics during a CMJ or drop jump can be measured by means of a 9 camera motion analysis system (VICON, 100Hz) and a force plate [
47] or the Motion Analysis Corporation 3D kinematic analysis system (200Hz) [
37]. Evaluated parameters of movement kinematics (jump height, maximal vertical ground reaction force, reactivity strength index, lower limb joint work) may serve as BMs of EIMUF [
47]. Other parameters of kinematic measurements by means of motion tracking systems include the mean and variability of joint angles, joint torque, and joint net movements for the shoulder, elbow, and wrist [
69]. These parameters usually decrease during fatigue. Increased kinematic variability may be found in the more proximal muscles and decreased kinematic variability in the more distal muscles [
69]. Kinematic and kinetic adaptations during fatigue are regarded as reactions to reduce biomechanical loading [
69].
Myo-mechanogram (MMG). A further tool to monitor EIMUF is the MMG, which measures the parameters peak torque, contraction time, relaxation time, the acceleration force development and relaxation, the slope and tau of force relaxation, and the mean power frequency fatigue threshold [
65,
70]. Peak torque, acceleration of force development, acceleration of relaxation, slope of force relaxation and tau of force relaxation decrease during EIMUF, while contraction time, relaxation time, and the tau of force relaxation increase [
70].
Muscle imaging. Functional analysis of muscles can be easily carried out by ultrasound. Particularly muscle fatigue of the diaphragm can be easily monitored by non-invasive ultrasound. A more elaborate method to monitor muscle fatigue is phosphorus magnetic resonance spectroscopy.
Scales and questionnaires. Numerous scores assessing fatigue during or after exercise are available. A major disadvantage of most of these scores is that the CNS component of muscle fatigue is included in the overall assessment of the performance decline after exercise. Further disadvantages are that they rely on subjective information and that many of these scales and questionnaires are not validated for the different types of exercise. Scores most frequently used to assess EIMUF are the perceived rating of fatigue scale [
45], the Borg rating perceived exertion (RPE) scale [
3], and the session rating of RPE (RPE multiplied by exercise duration). Others include the delayed-onset muscle soreness protocol, the delayed onset muscle soreness (DOMS) score [
43], and the Wingate test using the fatigue index [
21]. Disadvantage of the RPE is that it shows diurnal fluctuations with higher values at 17.00 h compared to 7.00 h [
50]. A further disadvantage of the RPE is that it is increased during submaximal tasks due to compensatory higher central and peripheral inputs [
10]. Additionally, physical and subjective changes in performance are less severe in real sport activities as compared to simulated activity [
10]. Other dry BMs could be psychomotor speed, monitoring of sleep quality, or the training impulse (TRIMP) [
3].