The Effects of Lower Extremity Static Muscle Fatigue on Balance Components

Abstract

Background: 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.

Objectives: This study investigated the effects of lower extremity static muscle fatigue on static and dynamic balance components. Design/Methods: 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 seconds, 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.

Results: There was a significant difference between pre-test and post-test Eyes Open (EO) static balance scores, pre- and post-exercise posttest dynamic balance scores between non-athletes and athletes, pre- and post-exercise posttest dominant leg EO, and pretest non-dominant leg between non-athletes and athletes (p<.05). There was a significant difference in the 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. There were statistically significant differences in the co-fatigue (coordinated fatigue) scores of the dominant leg agonist and antagonist muscle groups between non-athletes and athletes during isometric squat press (p<.05).

Conclusions: 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, and a co-fatigue index can help us investigate co-fatigue, especially during isometric effort at different knee joint angles and different joints.

1. Introduction

Cells communicate through electrical currents in millivolts or microvolts. We obtain and interpret the activations of electrical currents in the central nervous system and peripheral regions. These data provide important clues in terms of facilitating, developing, and explaining human life. Electrophysiological developments have gained importance to determine the chronic effects during exercise. In this context, new perspectives have been developed to measure electrical activations in muscles during sports activities and to analyze and interpret them correctly through appropriate methods. The brain perceives and interprets technical skills that differ across different types of exercises or sports. Responses to any sporting activity, exercise, or performance occur in muscles in line with the information sent from the brain. The examination of these responses in muscles is also of great importance [1].

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 (sEMG) is the most common method to achieve that [2]. Superficial electromyography is used for different purposes in rehabilitation, sports medicine, kinesiology, and sports sciences thanks to advances in electronics, electricity, computer science, and biomedicine. It is generally used to determine the physical load of muscle contraction, to identify muscle activation times, to define contraction profiles, and to describe fatigue formation in muscles [1]. It can be used alone or with different devices (isokinetic dynamometer, force platforms, image analysis, and balance platforms) [2].

The word “isometric” literally means “same length.” Static contraction and isometric contraction are used interchangeably. 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 [3].

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 [4, 5]. 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 [6]. There are two types of balance: static and dynamic. Static balance ensures that the body remains stable on a surface or position and remains in the desired position in the face of external forces or interventions. Hip stabilization plays a crucial role in providing and maintaining static balance. Stabilization and muscle coordination of all joints are necessary for balance and proper alignment [7]. All moving objects have dynamic balance [8]. Dynamic balance involves adjusting body position while performing activities (slowing down, accelerating, turning, etc.). The control of balance is dynamic when one is in motion [9, 10]. The base support surface refers to the surface between the feet and the ground that we need in order 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 [11, 12]. The stability limit refers to the angular area in which the center of gravity oscillates. In other words, it moves [13]. 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 in order 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 [14].

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 [15]. 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 [16].

This study examined the effects of static fatigue on static and dynamic balance components in lower extremity muscle groups.

2. Methods

3. 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 pretest and posttest ATE scores (p > 0.05).

There was a significant difference between pretest and posttest static balance EO scores (p < 0.05). However, there was no significant difference between pretest and posttest 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 posttest ATE scores between athletes and non-athletes (p<0.05). Non-athletes had a higher posttest ATE score than pretest ATE score, indicating poorer dynamic balance after exercise. Athletes had a significantly higher posttest ATE score than pretest 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 pretest non-dominant leg EO scores between athletes and non-athletes (p < 0.05). Athletes had a significantly higher pretest non-dominant leg EO score than non-athletes. Athletes had significantly higher posttest 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 pretest and posttest ATE scores than female participants (p < 0.05). The difference in the pretest dynamic balance components was significantly high (p < 0.01). The posttest 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 posttest non-dominant leg EO scores between male and female participants. Female participants also had a significantly lower mean posttest 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).

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 non-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 < 0.01). 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 non-dominant 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 non-athletes 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 non-athletes (p > 0.05).

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 non-athletes (p > 0.05).

Athletes had a significantly lower mean dominant leg agonist and antagonist muscle group co-fatigue score than non-athletes (p < 0.05). This result showed that the agonist and antagonist muscles of the athletes were fatigued at a similar rate during exercise compared to non-athletes.

There was no significant difference in the mean co-fatigue scores of the non-dominant leg agonist and antagonist muscle groups during isometric squat press between athletes and non-athletes (p > 0.05).

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).

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).

There was no significant difference in the mean dominant leg agonist and antagonist muscle co-fatigue scores between male and female participants during isometric squat press (p > 0.05).

There was no significant difference in the mean non-dominant leg agonist and antagonist muscle co-fatigue scores between male and female participants during isometric squat press (p > 0.05).

4. 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. People with poor balance are more likely to have difficulty performing desired movements, whereas those with good balance are more likely to succeed in physical performance and have a high quality of life. Balance functions highly in relation to skeletal muscles and neural mechanisms. People with dysfunctions or disabilities in those systems must go through rehabilitation to perform activities of daily living, to restore mobility and coordination, and to return to sports. Therefore, we learn about balance by specifying dynamic or static balance, determining the transition from dynamic to static state, and identifying differences between using dominant and non-dominant feet. These data allow us to find out whether the balance is at the desired level. With this information, we can identify exercises or rehabilitation processes, choose the right methods, and decide in what order to implement those methods in cases of dysfunctions or disabilities in balance. We can also use this information to help people with good balance to maintain their balance. If we use the right tests and devices to obtain data on balance, we can help athletes improve their performance or undergo rehabilitation in cases of dysfunctions or disabilities.

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. [19] 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 [20].

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 posttest ATE score than pretest 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 post-test 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. [21] investigated the effects of lower extremity isokinetic muscle fatigue on static balance and reported static balance deterioration after muscle fatigue. Rozzi et al. [22] 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. [23] 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 [24, 25, 26, 27].

Decreases in mean frequency (MF) 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 [28]. 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 non-athletes 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 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 non-dominant 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 [29] 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 medailis 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 [30, 31, 32, 33]. 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 [30, 31]. Some of the mechanisms that contribute to changes in muscle force generation during fatigue are metabolite accumulation [33, 34, 35], inhomogeneous activation [36], and changes in Ca²⁺ concentration and sensitivity [37, 38]. In addition, an increase in antagonist muscle activity during sustained isometric contraction may exacerbate fatigue in the agonist muscles [39]. Changes in ankle angle during an isometric contraction [40, 41] may affect the fascicle length [42], and thus, the force potential of the muscle due to force. The pennation angle is a component of the force that acts through muscle fibers horizontally and orthogonally to the tendon. Changes in the pennation angle are regarded as an increase in this angle during isometric contraction, which leads to a reduction in force transmission to the tendon.

There was a significant difference in the mean co-fatigue scores of the dominant leg agonist and antagonist muscle groups between athletes and non-athletes during isometric squat press exercise. This result showed that athletes experienced more similar fatigue in the agonist and antagonist muscles during exercise than non-athletes. There was no significant difference in the mean co-fatigue scores of the non-dominant leg agonist and antagonist muscle groups between athletes and non-athletes during isometric squat press exercise. There was no significant difference in the mean co-fatigue scores of the dominant leg agonist and antagonist muscle groups between male and female participants during isometric squat press exercise. There was no significant difference in the mean co-fatigue scores of the non-dominant leg agonist and antagonist muscle groups between male and female participants during isometric squat press exercise. Agonist and antagonist co-fatigue play an important role in stabilizing the knee joint after fatigue. However, it is still unclear whether selective fatigue of agonist or antagonist muscles causes changes in muscle activation patterns. Determining the co-fatigue levels of agonist and antagonist muscles indirectly affects muscle activation, which is an important factor affecting exercise efficiency because it depends on muscle activation levels at the moment of maximum contraction during voluntary contraction [18].

5. Conclusions

Above all, we should ensure that motor skills are fully and harmoniously developed at every stage to turn non-athletes into well-trained athletes. 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.

Surface EMG is a non-invasive source of information regarding the status of skeletal muscle fatigue. Numerous practical biomechanical methods show that interdisciplinary bioengineering approaches are successful in providing quantitative EMG-based information on the fatigue state of skeletal muscles. If we integrate advanced measurement techniques with sophisticated mathematical methods and digital signal processing techniques, we can establish a solid foundation for standardizing methods suitable for biomechanical situations. We foresee those biomechanical methods will be improved, standardized, and implemented in the future. Modern methods in a new muscle fatigue monitoring device have not yet been standardized in clinical diagnostic practice both in sports and medical rehabilitation processes.

A co-fatigue index can help us determine efficiency in sports branches. It is important to identify co-fatigue, especially during isometric contractions. A co-fatigue index can help us investigate co-fatigue, especially during isometric effort at different knee joint angles and different joints.

Declarations

Acknowledgment

The authors thank all the participants involved in the study, for their patience and committed involvement. This paper is derived from the master's thesis written by Can AKYILDIZ. 

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The study was supported by the Scientific Research Projects Coordination Unit of Ordu University (B-1906).

Ethics Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the Clinical Research Ethics Committee of Ordu University (KAEK-216).

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Authors’ contribution

All authors listed have made a substantial, direct, and intellectual contribution to the work, and approved it for publication.

References

1. Cerrah A. (2010) Spor Bilimlerinde Elektromiyografi Kullanımı, Sportmetre Beden Eğitimi ve Spor Bilimleri Dergisi VIII (2) 43–49. https://doi.org/10.1501/Sporm_0000000175
2. Türker, H., Sozen, H. (2013) Surface electromyography in sports and exercise. Electrodiagnosis in new frontiers of clinical research, 175–194. http://dx.doi.org/10.5772/56167
3. Clifford, C., Challoumas, D., Paul, L., Syme, G., & Millar, N. L. (2020) Effectiveness of isometric exercise in the management of tendinopathy: a systematic review and meta-analysis of randomised trials. BMJ open sport & exercise medicine, 6(1), e000760. http://dx.doi.org/10.1136/bmjsem-2020-000760
4. Winter, D. A., Patla, A. E., Ishac, M., Gage, W. H. (2003) Motor mechanisms of balance during quiet standing. Journal of electromyography and kinesiology, 13(1), 49–56. https://doi.org/10.1016/S1050-6411(02)00085-8
5. Sözen H., Akyıldız C. (2019) Spor Bilimlerinde Denge ve Dengenin Değerlendirilmesi. S. 143–157 10. Bölüm/ Gece Akademi /Ankara. ISBN • 978-605-7749-91-8
6. Cote, K.P., Brunet, M. E., Gansneder, B. M. and Shultz, S. J. (2005) Effects of pronated and supinated foot postures on static and dynamic postural stability. Journal of athletic training, 40(1), 41.
7. Ackland, T.R., Elliott, B. and Bloomfield, J. (2009) Applied anatomy and biomechanics in sport. Human Kinetics.
8. Muratlı, S.; Toraman, F.; Çetin, E. (2000) Sportif Hareketlerin Biomekanik Temelleri, Bağırgan Yayımevi, Ankara. S.37–90.
9. Chaudhari AM, Andriacchi TP. (2006) The mechanical consequences of dynamic frontal plane limb aligment for non-contact acl injury. JBiomech, 39(2): 330–338. https://doi.org/10.1016/j.jbiomech.2004.11.013
10. Aktümsek, A. (2012) Anatomi ve Fizyoloji, İnsan Biyolojisi. Nobel Yayın Dağıtım, Ankara.
11. Duncan P.W., Weiner D. K., Chandler J., Studentski S. (1990) Functional reach: a new clinical measure of balance. J Gerontol,45(6):192–197. https://doi.org/10.1093/geronj/45.6.M192
12. Minton, S.C. (2003) Dance, Mind & Body. Human Kinetics. ERIC.
13. McCollum, G. and Leen, T.K. (1989) Form and exploration of mechanical stability limits in erect stance. Journal of Motor Behavior, 21(3), 225–244. https://doi.org/10.1080/00222895.1989.10735479
14. Piker, E. G., Jacobson, G. P., Newman, C. W. (2020) Assessing Dizziness-Related Quality of Life. Balance Function Assessment and Management, 143.
15. Rogind, H., Simonsen, H., Era, P., Bliddal, H. (2003) Comparison of Kistler 9861a Force Platform and Chattecx Balance System® for Measurement of Postural Sway: Correlation and Test–Retest Reliability. Scandinavian Journal of Medicine & Science in Sports, 13(2), 106–114. https://doi.org/10.1034/j.1600-0838.2003.01139.x
16. Tjernström, F., Fransson, P. A., Hafström, A., Magnusson, M. (2002) Adaptation of Postural Control to Perturbations—A Process That Initiates Long-Term Motor Memory. Gait & Posture, 15(1), 75–82. https://doi.org/10.1016/S0966-6362(01)00175-8
17. De Luca, C. J. (1984) Myoelectrical Manifestations of Localized Muscular Fatigue in Humans. CRC Critical Reviews in Biomedical Engineering, 11(4):251–279.
18. Sozen, H., Erdogan, E., Ince, A., Soylu, A. R. (2019) Determination of Electromyography-Based Coordinated Fatigue Levels in Agonist and Antagonist Muscles of the Thigh during Squat Press Exercise. Annals of Applied Sport Science, 7(3), 21–30. https://doi.org/10.29252/aassjournal.738
19. Merletti, R., Farina D. (2006) Myoelectric Manifestations of Muscle Fatigue. In Wiley Encyclopedia of Biomedical Engineering. New York: American Cancer Society. https://doi.org/10.1002/9780471740360.ebs1427
20. Cifrek, M., Medved, V., Tonković, S., Ostojić, S. (2009) Surface EMG based muscle fatigue evaluation in biomechanics. Clinical biomechanics, 24(4), 327–340. https://doi.org/10.1016/j.clinbiomech.2009.01.010
21. Kwon, O. Y., Choi, H. S., Yi, C. H., Kwon, H. C. (1998) The effects of knee and ankle muscles surrounding the knee and ankle joints on one-leg static standing balance. Journal of Physical Therapy Science, 10(1), 7–12. https://doi.org/10.1589/jpts.10.7
22. Rozzi, S. L., Lephart, S. M., Fu, F. H. (1999) Effects of muscular fatigue on knee joint laxity and neuromuscular characteristics of male and female athletes. Journal of athletic training, 34(2), 106. https://doi.org/10.1177/03635465990270030801
23. Fatahi, M., Ghasemi, G. A., Mongashti Joni, Y., Zolaktaf, V., Fatahi, F. (2016) The effect of lower extremity muscle fatigue on dynamic postural control analyzed by electromyography. 6(1), 37–50.‎
24. Bringoux, L., Marin, L., Nougier, V., Barraud, P. A., Raphel, C. (2000) Effects of gymnastics expertise on the perception of body orientation in the pitch dimension. Journal of Vestibular Research, 10(6), 251–258. https://doi.org/10.3233/VES-2000-10602
25. Karakaya, MG., Rutbil, H., Akpinar, E., Yildirim, A., Karakaya, IC. (2015) Effect of ankle proprioceptive training on static body balance. Journal of physical therapy science, 27(10), 3299–3302. https://doi.org/10.1589/jpts.27.3299
26. Çankaya, S., Gokmen, B., Tasmektepligil, M. Y., Con, M. (2015) Special balance developer training applications on young males’ static and dynamic balance performance. The Anthropologist, 19(1), 31–39. https://doi.org/10.1080/09720073.2015.11891636
27. Conner, B. C., Petersen, D. A., Pigman, J., Tracy, J. B., Johnson, C. L., Manal, K., Crenshaw, J. R. (2019) The cross-sectional relationships between age, standing static balance, and standing dynamic balance reactions in typically developing children. Gait & posture, 73, 20–25. https://doi.org/10.1016/j.gaitpost.2019.07.128
28. Allison, G. T., Fujiwara, T. (2002) The relationship between EMG median frequency and low frequency band amplitude changes at different levels of muscle capacity. Clinical Biomechanics, 17(6), 464–469. https://doi.org/10.1016/S0268-0033(02)00033-5
29. Mademli, L., Arampatzis, A. (2005) Behaviour of the human gastrocnemius muscle architecture during submaximal isometric fatigue. European journal of applied physiology, 94(5–6), 611–617. https://doi.org/10.1007/s00421-005-1366-8
30. Bigland-Ritchie, B., Cafarelli, E., Vollestad, N. K. (1986) Fatigue of submaximal static contractions. Acta Physiol Scand Suppl, 556, 137–148.
31. Garland, S. J., Enoka, R. M., Serrano, L. P., Robinson, G. A. (1994) Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. Journal of Applied Physiology, 76(6), 2411–2419. https://doi.org/10.1152/jappl.1994.76.6.2411
32. Hunter, S. K., Enoka, R. M. (2003) Changes in muscle activation can prolong the endurance time of a submaximal isometric contraction in humans. Journal of Applied Physiology, 94(1), 108–118. https://doi.org/10.1152/japplphysiol.00635.2002
33. De Groot, M., Massie, B. M., Boska, M., Gober, J., Miller, R. G., Weiner, M. W. (1993) Dissociation of [H+] from fatigue in human muscle detected by high time resolution 31P-NMR. Muscle & Nerve: Official Journal of the American Association of Electrodiagnostic Medicine, 16(1), 91–98. https://doi.org/10.1002/mus.880160115
34. Miller, R. G., Giannini, D., Milner-Brown, H. S., Layzer, R. B., Koretsky, A. P., Hooper, D., Weiner, M. W. (1987) Effects of fatiguing exercise on high‐energy phosphates, force, and EMG: evidence for three phases of recovery. Muscle & Nerve: Official Journal of the American Association of Electrodiagnostic Medicine, 10(9), 810–821. https://doi.org/10.1002/mus.880100906
35. Boska, M. D., Moussavi, R. S., Carson, P. J., Weiner, M. W., Miller, R. G. (1990) The metabolic basis of recovery after fatiguing exercise of human muscle. Neurology, 40(2), 240–240. https://doi.org/10.1212/WNL.40.2.240
36. Huijing, P. A. (1998) Muscle, the motor of movement: properties in function, experiment and modelling. Journal of Electromyography and Kinesiology, 8(2), 61–77. https://doi.org/10.1016/S1050-6411(97)00023-0
37. Cooke, R., Pate, E. (1985) The effects of ADP and phosphate on the contraction of muscle fibers. Biophysical journal, 48(5), 789–798. https://doi.org/10.1016/S0006-3495(85)83837-6
38. Allen, D. G., Lannergren, J., Westerblad, H. (1995) Muscle cell function during prolonged activity: cellular mechanisms of fatigue. Experimental Physiology: Translation and Integration, 80(4), 497–527. https://doi.org/10.1113/expphysiol.1995.sp003864
39. Psek, J. A., Cafarelli, E. (1993) Behavior of coactive muscles during fatigue. Journal of Applied Physiology, 74(1), 170–175. https://doi.org/10.1152/jappl.1993.74.1.170
40. Magnusson, S. P., Aagaard, P., Rosager, S., Dyhre-Poulsen, P., Kjaer, M. (2001) Load‐displacement properties of the human triceps surae aponeurosis in vivo. The Journal of physiology, 531(1), 277–288. https://doi.org/10.1111/j.1469-7793.2001.0277j.x
41. Muramatsu, T., Muraoka, T., Takeshita, D., Kawakami, Y., Hirano, Y., Fukunaga, T. (2001) Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo. Journal of Applied Physiology, 90(5), 1671–1678. https://doi.org/10.1152/jappl.2001.90.5.1671
42. Narici, M. V., Binzoni, T., Hiltbrand, E., Fasel, J., Terrier, F., Cerretelli, P. (1996) In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. The Journal of physiology, 496(1), 287–297. https://doi.org/10.1113/jphysiol.1996.sp021685