The effects of lower extremity static muscle fatigue on balance components

The body exhibits dynamic and static movements in response to the changes in the center of gravity in some positions. Balance plays a key role in all sports branches and daily life because it can control the lowest energy consumption and muscle activation. This study investigated the effects of lower extremity static muscle fatigue on static and dynamic balance components. The sample consisted of 40 healthy volunteers aged 18–24 years. Participants took part in an isometric fatigue protocol for lower extremity muscles. A squat position was used for static fatigue for lower extremity muscles. Measurements were performed in a squat press for 25 s, with the knee at a 90-degree angle and a load of about 30% of the participant's weight isometrically. The protocol was repeated five times. The participant was allowed to rest for two minutes between each repetition. The muscles and their antagonists that contracted most actively during the squat press exercise were vastus lateralis obliquus, rectus femoris, tibialis anterior, biceps femoris, semi tendineus, and lateral gastrocnemius. Electromyography (EMG) measurements were conducted on these muscles bilaterally and motion analysis system was used to standardize the 90-degree angle of the knee joint. There was a significant difference between pre-test and post-test Eyes Open (EO) static balance scores, pre- and post-exercise post-test dynamic balance scores between non-athletes and athletes, pre- and post-exercise post-test dominant leg EO, and pre-test non-dominant leg between non-athletes and athletes (p < .05). There was a significant difference in the Median Frequency (MF) (Hz) values of the dominant leg agonist rectus femoris (p < .05) and the antagonist muscle semi tendineus (p < .05) scores during isometric squat press between athletes and non-athletes. We need different applications to understand the mechanisms underlying balance and discover athletes' potential. Lower extremity proprioception exercises have positive effects on static body balance parameters.


Introduction
Most movements become automatic after they are consciously learned, and therefore, it is hard to correct motor skills that are incorrectly automated. Athletes or non-athletes who take measures at a young age are more likely to learn motor skills correctly. We need to define and practice each motor skill required for each activity, formation, and technical movement. Superficial electromyography is the most 1 3 common method to achieve that. It can be used alone or with different devices (isokinetic dynamometer, force platforms, image analysis, and balance platforms) [1].
In isometric contraction, the internal tension produced by the muscle is less than the external resistance, and therefore, there is no change in the joint angle and muscle length. However, the muscle tension, that is, the tone, increases. Muscles always contribute directly to the formation of the relevant joint movement. Muscles can cause or prevent movement. Standing upright and arm wrestling despite gravity are the best examples for this situation [2].
Balance detects and regulates sensory stimuli and plans movements for upright posture. Balance is the ability to control the body with minimal energy consumption and minimal muscle activation in dynamic and static positions in response to possible changes in the center of gravity. The primary balance mechanism is to minimize the forces acting on the body and preserve its alignment in response to internal and external forces [3,4]. The balance mechanism requires the skeletal and neural systems to work regularly. This rhythmic action is provided by the transmission, collection, evaluation, and rhythmic execution of vestibular, visual, and proprioceptive senses in the central nervous system [5]. Stabilization and muscle coordination of all joints are necessary for balance and proper alignment [6]. The base support surface refers to the surface between the feet and the ground that we need to have the desired posture. If the base support surface is uneven or smaller than the object, the support is reduced. Therefore, if the base support surface is uneven or narrow, the balance shows a negative trend [7,8]. The stability limit refers to the angular area in which the center of gravity oscillates. In other words, it moves [9]. The limit of this area depends on the base support surface position and the position of the feet. When an average person is in a relaxed standing position, the limit of stability is elliptical. The body must be able to continuously regulate the displacements of the center of gravity in response to internal and external forces and keep it within the limits of stability for balance. One performs oscillations in various directions to maintain balance. Any oscillation, voluntarily or otherwise, made by the center of gravity is called the oscillation limit. Sensory state and its relationship with the support surface are effective in this case [10].
The main task of the balance system is to maintain the vertical projection of the body's center of gravity within the base support area. This is the case because the body is not rigid, but it experiences constant oscillations on its vertical projection [11]. Stable balance depends on a feedback control mechanism, which is a complex system governed by receptors of the visual, vestibular, and somatosensory systems that receive various stimuli [12]. Postural control for stability and orientation requires afferent input to produce the appropriate torque in maintaining body position, and injury to the neck and/or otolith structures affecting the afferent has been suggested. Feedback can contribute to this loss of balance. Sensory modalities involved in maintaining balance include somatoafferent, vestibular, and visual input to assess current body position, as well as external disturbances and feedback to previous efferent strategies. As a result, the motor process coordinates the trunk and lower extremity muscles into combined postural strategies to reduce body sway and keep it on the base of support [13]. Despite the low energy cost, isometric contraction can lead to the onset of local muscle fatigue. The onset of fatigue occurs faster when the relative force applied is greater than 15-20% of the maximum voluntary contraction of the muscle being considered and the duration of contraction increases. Ischemia promotes the accumulation of acid metabolites produced during contraction and inhibits their elimination, thus forming the main causative factor in the onset of local muscle fatigue. Initiating periods of rest of sufficient duration to restore normal blood flow through the muscle is an effective way to delay or even prevent the onset of muscle fatigue [14]. It was seen that it was affected by many different factors when the physiological basis of balance was examined Static fatigue may also be one of these factors. Because static fatigue is a level of fatigue that occurs in muscle tension without causing a change in muscle length. Static stretching, which is frequently used especially in archery, weightlifting, judo, wrestling, and gymnastics, can cause changes in fatigue levels and balance parameters. This study examined the effects of static fatigue on static and dynamic balance components in lower extremity muscle groups.

Study design
The sample consisted of 40 healthy volunteers (ten male athletes, ten female athletes, ten non-athlete men, and ten non-athlete females) aged 18-24 years.

Data collection
Participants took part in an isometric fatigue protocol for lower extremity muscles. A squat position was used for static fatigue for lower extremity muscles. Measurements were performed in a squat press for 25 s, with the knee at a 90-degree angle and a load of about 30% of the participant's weight isometrically. The isometric squat protocol we used in our study is a modified form of the lower extremity isometric fatigue protocols used in different studies [15][16][17][18][19]. The protocol was repeated five times. The participant was allowed to rest for two minutes between each repetition. The muscles and their antagonists that contracted most actively during the squat press exercise were vastus lateralis obliquus, rectus femoris, tibialis anterior, biceps femoris, semi tendineus, and lateral gastrocnemius. EMG measurements were conducted on these muscles bilaterally. EMG data were recorded during each exercise protocol using wireless surface Ag/AgCl electrodes and a Noraxon device (myo-MUSCLE, Noraxon, Scottsdale, AZ, USA). Noraxon (myo-MOTION, Noraxon, Scottsdale, AZ, USA) motion analysis system was used to standardize the 90-degree angle of the knee joint. All muscle electrode locations were selected in accordance with the SENIAM criteria ( Fig. 1).

Electromyography analysis
Electromyography data were passed through a 20 Hz highpass Butterworth filter, and then, the median frequency was calculated (Hz) between 5 and 20 s of motion. The data were filtered at 20 Hz high-pass Butterworth filter slope was selected because it exhibited less overshoot and has a faster settling time in response to signal transients [20]. Muscle fatigue studies using EMG signals focus on median frequency to calculate the fatigue index. The median frequency divides two equal parts of the total power spectral area. The more fatigued the muscle, the lower the MF during isometric contraction [21].

Balance measurements
The static and dynamic balance were measured before and after the fatigue protocol. The static and dynamic balance were measured using a CSI TecnoBody (PK-252) balance system, which provides objective and measurable data. The system is run by servo motors (air pistons) and measures the dynamic balance at an operating angle of 15 degrees in all directions of the platform. Dynamic balance results can be monitored and recorded live on a screen on the device. The balance of the moving platform is automatically adjusted by the weight applied to each point of the platform and the coefficient of instability. Therefore, the platform applies different resistance to everyone. In other words, everyone encounters resistance according to their weight. This feature allows us to compare measurement outcomes regardless of weight. The automatic motor locking function allows the device to switch from dynamic measurement to static measurement instantly.

Static balance measurements
Static test balance measurements were performed in two ways: eyes open (EO) and eyes closed (EC). They were made on a flat surface and a stable platform on two legs. The participant's feet were shoulder-width apart. The feet were positioned in such a way that the x and y axes on the platform were equidistant from the origin point determined as a reference to the lines indicating the oscillation zones. The test lasted 30 min. The participant was asked to maintain his/her position during the test. The static balance measurement protocol was started by clicking the start button on the device screen. The device automatically terminated the test.
Static  Area Used (mm 2 ) [22]. Static EO, EC, dominant leg, and non-dominant leg balance scores were the sum of the rightleft standard deviation and the forward-backward standard deviation. Higher balance scores indicated poorer balance, whereas lower balance scores indicated better balance.

Dynamic balance measurements
Dynamic test balance measurements were performed on a flat surface and a stable platform on two legs. The participant's feet were shoulder-width apart. The feet were positioned in such a way that the x and y axes on the platform were equidistant from the origin point determined as a result of reference to the lines indicating the oscillation zones. The circular oscillating movements of the body were followed clockwise. The specific route on the circular shape on the device screen was completed by turning five rounds for 60 s, provided that the feet remained on the floor. The device automatically terminated the test at the end of the fifth round. Some participants could not complete the test in 60 s. Their balance scores were the scores they obtained until the moment the test was over.
Dynamic balance data are referred to as Average Track Error (ATE). The resulting values show the amount of deviation or exceedance of the limits of the path that the participant should follow. Higher ATE scores indicated poorer dynamic balance, while lower ATE scores indicated better dynamic balance.

Statistical analysis
The data were analyzed using the Statistical Package for Social Sciences (SPSS, v. 22.0) at a significance level of 0.05. Arithmetic mean (X) and standard deviation (Sd) were used for descriptive statistics. The Shapiro-Wilk test was used for normality testing, and the results showed that the data were normally distributed. Therefore, an independent samples t-test was used to determine comparing the median frequency scores of the effects of fatigue levels on the static and dynamic balance between groups (athletes-non-athletes; males-females). A paired-samples t-test was used to compare pre-test and post-test static and dynamic balance sores.

Results
There was no significant difference in body height, body weight, age, Body Mass Index, body fat percentage, lean body mass, soft lean mass, skeletal muscle mass, total body water, and protein levels between non-athletes and athletes (p > 0.05). This result indicated that the two groups were homogenous.
There was no significant difference between pre-test and post-test ATE scores (p > 0.05).
There was a significant difference between pre-test and post-test static balance EO scores (p < 0.05). However, there was no significant difference between pre-test and post-test Static EC, dominant single leg, and non-dominant single leg static balance scores (p > 0.05). These results showed differences only in the static EO balance scores after exercise, indicating improvements in static EO balance values after exercise.
There was a significant difference in the post-test ATE scores between athletes and non-athletes (p < 0.05). Nonathletes had a higher post-test ATE score than pre-test ATE score, indicating poorer dynamic balance after exercise. Athletes had a significantly higher post-test ATE score than pre-test ATE score, indicating poorer dynamic balance after exercise. There was no significant difference in pretest balance components between athletes and non-athletes (p > 0.05).
There was a significant difference in the pre-test nondominant leg EO scores between athletes and non-athletes (p < 0.05). Athletes had a significantly higher pre-test nondominant leg EO score than non-athletes. Athletes had significantly higher post-test dominant leg EO and non-dominant EO static balance scores than non-athletes (p < 0.05). There was no significant difference in the other static balance components between athletes and non-athletes (p > 0.05).
Male participants had significantly lower pre-test and post-test ATE scores than female participants (p < 0.05). The difference in the pre-test dynamic balance components was significantly high (p < 0.01). The post-test dynamic balance scores showed that male participants had poorer dynamic balance after exercise but that their scores were better compared to female participants' scores.
Female participants had a significantly lower mean pretest non-dominant leg EO score than male participants (p < 0.05). However, there was no significant difference in the post-test non-dominant leg EO scores between male and female participants. Female participants also had a significantly lower mean post-test dominant leg EO score than their male counterparts (p < 0.05). There were no significant differences in the other static balance scores between male and female participants (p > 0.05) ( Tables 1, 2, 3 , 4, 5, 6, 7, 8, 9).
This study compared the MF (Hz) scores of the dominant leg agonist and antagonist muscles in athletes and non-athletes during isometric squat press (average of five repetitions). When we focused on the muscles involved in the exercise, we saw a significant difference in the rectus femoris, an agonist muscle (p < 0.05). Non-athletes had a significantly lower agonist rectus femoris MF score than athletes. This result showed that non-athletes experienced more fatigue than athletes during exercise. Of the antagonist muscles, we observed a significant difference only in semi     tendineus (p < 0.05). Non-athletes had a significantly lower agonist semi tendineus MF score than athletes. This result also showed that non-athletes experienced more fatigue than athletes during exercise. There were no significant differences in the MF scores of the other dominant leg agonist and antagonist muscles (p > 0.05). This study compared the MF (Hz) scores of the nondominant leg agonist and antagonist muscles in athletes and non-athletes during isometric squat press (average of five repetitions). When we focused on the muscles involved in the exercise, we saw a significant difference in the rectus femoris, an agonist muscle (p < 0.01). Non-athletes had a significantly lower agonist rectus femoris MF score than athletes. This result showed that non-athletes experienced more fatigue than athletes during exercise. There were no significant differences in the MF scores of the other nondominant leg agonist and antagonist muscles (p > 0.05). Table 10 compares the mean MF (Hz) scores of the dominant leg agonist and antagonist muscles in athletes and nonathletes during isometric squat press exercise. Non-athletes had significantly lower mean antagonist muscle MF (Hz) scores than athletes (p < 0.05). This result showed that non-athletes experienced more fatigue than athletes during exercise. There was no significant difference in the mean MF scores of the muscle groups between athletes and nonathletes (p > 0.05) (Tables 11, 12, 13). There was no significant difference in the mean MF (Hz) scores of the non-dominant leg agonist and antagonist muscles during isometric squat press between athletes and nonathletes (p > 0.05).
Supplementary Table 14 compares the mean dominant leg agonist and antagonist muscle MF (Hz) scores in male and female participants during isometric squat press exercise. Female participants had significantly lower mean dominant leg agonist muscle MF (Hz) scores than male participants (p < 0.05). This result showed that female participants experienced more fatigue in their agonist muscle groups than their male counterparts during isometric squat press exercise. Female participants also had lower mean dominant leg antagonist muscle MF (Hz) scores than male participants (p = 0.080), but the difference was statistically insignificant (p > 0.05).
Supplementary Table 15 compares the mean non-dominant leg agonist and antagonist muscle MF (Hz) scores in male and female participants during isometric squat press exercise. There was no significant difference in agonist muscle MF (Hz) scores between male and female participants during isometric squat press exercise (p > 0.05). Although female participants had lower mean non-dominant leg antagonist muscle MF (Hz) scores than male participants (p = 0.057), the difference was statistically insignificant (p > 0.05).

Discussion
Balance is the ability of the body to maintain its position on a support surface with as little movement as possible. Joint positions required to perform the desired function, muscles working in harmony, and the conservation of the center of gravity are also the ability of the body to maintain physical adaptation in response to changing situations. Balance plays an important role in maintaining physical performance and daily life under desired conditions.
Muscle fatigue is a complex chain of events involving different causes and mechanisms. Fatigue results from metabolic and structural changes in the muscles due to insufficient oxygen and malnutrition and the changes in the efficiency of the nervous system. Merletti and Farina et al. [23] group the sites of fatigue under the headings of (1) central fatigue, (2) fatigue of the neuromuscular junction, and (3) muscle fatigue. The term "muscle fatigue," which means "local muscle fatigue," is also expressed or equivalent to "neuromuscular" fatigue [24]. This study investigated the effects of lower extremity static muscle fatigue on balance components. The athletes and non-athletes in this study had similar physiological characteristics. Therefore, the groups were homogenous, suggesting that similar physiological characteristics would not affect physiological responses.
This study focused on Average Track Error (ATE) as a dynamic balance component to investigate pre-test and post-test dynamic balance scores. There was no significant difference between pre-test and post-test dynamic balance scores. There was a significant difference between pre-test and post-test static balance EO scores. However, there was no significant difference between pre-test and post-test Static EC, dominant single leg, and non-dominant single leg static balance scores. These results showed only significant differences in static EO balance scores after exercise. This difference indicated improvements in static EO balance scores after exercise. There was a significant difference in ATE scores between athletes and non-athletes. Non-athletes had a higher post-test ATE score than pre-test ATE score, but the difference was statistically insignificant. On the other hand, athletes had a significantly higher post-test ATE score than pre-test ATE score, indicating that their dynamic balance components worsened more after exercise. There was no significant difference in pre-test balance components between athletes and non-athletes. Non-athletes had a significantly lower mean pre-test non-dominant leg EO score than athletes. Non-athletes also had significantly lower mean dominant leg EO and non-dominant EO static balance scores than athletes. There was no significant difference in EO and EC scores between athletes and non-athletes. Male participants had significantly lower pre-test and posttest ATE scores than female participants. The difference in pre-test ATE scores between male and female participants was significantly high. These results showed that although male participants had worse dynamic balance scores after exercise, they had better scores than their female counterparts. Female participants had a significantly lower mean pre-test non-dominant leg EO score than male participants. However, there was no significant difference in post-test non-dominant leg EO scores between male and female participants. Female participants also had a significantly lower mean post-test dominant leg EO score than male participants. There was no significant difference in the other static balance scores between male and female participants. Kwon et al. [25] investigated the effects of lower extremity isokinetic muscle fatigue on static balance and reported static balance deterioration after muscle fatigue. Rozzi et al. [26] used electromyography to determine fatigue in six muscle groups responsible for knee joint stability. They reported reductions in stability index and proprioceptive abilities in both sexes. Fatahi et al. [27] compared the electromyography activity of the lower extremity muscle groups before and after fatigue.
They reported increases in electromyography activations in the muscle groups close to the knee joint after fatigue. They concluded that muscle fatigue increased the sensitivity of the joints and thus made postural control difficult. Research shows that athletes who participate in training programs to improve balance performance have better balance components than non-athletes [28][29][30][31].
Decreases in mean frequency in surface EMG profiles are used to determine fatigue (high frequency) in an isometric muscle movement. Methods used to generate MF data often rely on fixed waveforms and high sampling rates [32]. This study examined the mean differences in the MF (Hz) scores of the dominant leg agonist and antagonist muscles in athletes and non-athletes during a five-repetition isometric squat press exercise. Considering the muscles involved in the exercise, we observed a statistical difference in the rectus femoris, an agonist muscle. This result showed that nonathletes had a lower MF score in the rectus femoris than athletes, indicating that non-athletes experienced more fatigue during exercise. Of the antagonist muscles, the only difference was observed in the semi tendineus. Non-athletes had a lower MF score in the semi tendineus than athletes, indicating that non-athletes experienced more fatigue during exercise. There was no significant difference in the MF scores in the other dominant leg agonist and antagonist muscles. This study examined the mean differences in the MF (Hz) scores of the non-dominant leg agonist and antagonist muscles in athletes and non-athletes during the five-repetition isometric squat press exercise. Considering the muscles involved in the exercise, we observed a statistical difference in the rectus femoris. This result showed that non-athletes had a lower MF score in the rectus femoris than athletes, indicating that non-athletes experienced more fatigue during exercise. There was no significant difference in MF scores in the other non-dominant leg agonist and antagonist muscles. This study examined the mean differences in MF (Hz) scores of the dominant leg agonist and antagonist muscles in athletes and non-athletes during isometric squat press. Non-athletes had significantly lower mean scores in antagonist muscle groups than athletes, indicating that non-athletes experienced more fatigue in the antagonist muscle groups during exercise than athletes. There was no significant difference in the MF scores of the agonist muscle groups between athletes and non-athletes. This study examined the mean differences in the MF (Hz) scores of the non-dominant leg agonist and antagonist muscles in athletes and non-athletes during isometric squat press. There was no significant difference in the MF (Hz) scores of the non-dominant leg agonist and antagonist muscles between athletes and non-athletes. This study looked into the mean differences in the MF (Hz) scores of the non-dominant leg agonist and antagonist muscles in male and female participants during isometric squat press. Female participants had a significantly lower MF (Hz) score in the 1 3 agonist muscle groups than male participants. This result showed that female participants experienced more fatigue in the agonist muscle groups than male participants during exercise. Female participants had a lower MF (Hz) score in the antagonist muscle groups than male participants, but the difference was statistically insignificant. This study investigated the mean differences in the MF (Hz) scores in the nondominant leg agonist and antagonist muscles in male and female participants during isometric squat press exercise. There was no significant difference in the MF (Hz) scores in the non-dominant leg agonist muscles between male and female participants during isometric squat press exercise. Female participants had lower MF (Hz) scores in the antagonist muscle groups than male participants, but the difference was statistically insignificant. Mademli and Arampatzis [33] used EMG to investigate the fatigue level of the gastrocnemius medialis in isometric plantar flexion angle. They found that changes in fascicle length and pennation angle of gastrocnemius medialis during contraction affected the strength potential of the muscle due to the force-length relationship and the transfer of force to the tendon. They presented evidence that this might contribute to the increase in the EMG activity of the gastrocnemius medialis during submaximal isometric sustained contractions. These results are similar to ours. Our result also showed that the decrease in the fascicle length of the muscles involved in the continuous isometric contraction increased muscle fatigue. This was observed with an increase in the EMG activity of the muscles and a decrease in the MF scores. EMG activity usually increases gradually for a given force during a submaximal isometric contraction [34][35][36][37]. This increase suggests that the body involves more motor units to make up for the inability of the currently active muscle fibers to maintain force generation [34,35]. Some of the mechanisms that contribute to changes in muscle force generation during fatigue are metabolite accumulation [37][38][39], inhomogeneous activation [40], and changes in Ca 2+ concentration and sensitivity [41,42]. In addition, an increase in antagonist muscle activity during sustained isometric contraction may exacerbate fatigue in the agonist muscles [43]. Changes in ankle angle during an isometric contraction [44,45] may affect the fascicle length [46], and thus, the force potential of the muscle due to force. Affecting the strength potential of the muscle may also cause destabilization of the joint and deterioration in the balance components of the body.

Conclusions
Some researchers focus on possible strategies to improve athletes' static and dynamic balance and the impact of different sports activities on postural strategies at an early age. Balance is a complex composition. Therefore, we need different applications to understand the mechanisms underlying balance and discover athletes' potential. Lower extremity proprioception exercises have positive effects on static body balance parameters. In future studies, it may be recommended to examine individuals of different ages with different muscle fatigue protocols.