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1. Introduction
Lower extremity injuries are common in sports [1]. Volleyball is a non-contact sport in which non-traumatic injuries prevalently occur due to long durations of playing which induce fatigue [2]. Fatigue of lower extremity muscles could happen following the changes in neuromuscular control; they may lead to imbalance [3] and predisposition to injuries. 
In sports activities, like volleyball, dynamic balance is necessary to ensure instantaneous reaction to the changing environment [4, 5, 6]. Fatigue is a major factor that influences athletes’ performance during the competition [7]. Exercise-induced reduction in voluntary muscle activation is described as fatigue [4]. Due to the accumulation of metabolites in muscles, the most common time for injuries to occur may be in the final sets of the matches on account of the onset of fatigue [8, 9, 10, 11]. Numerous studies have reported the effects of muscular fatigue on static balance [12, 13, 14] and dynamic balance [13, 15] in different populations. However, fatigue is induced by various patterns, either locally or generally. There exist several jumping and landing movements in volleyball, especially during spike and block actions. Various muscular groups are activated during these actions, particularly hip extensors, knee extensors, and ankle Plantar Flexors (PFs). Thus, it is essential to assess the impact of these muscles’ fatigue on dynamic balance in volleyball players.
The Star Excursion Balance Test (SEBT) is a feasible and reliable tool for assessing dynamic balance. The SEBT can be integrated into physical examinations to estimate the risk of injury in athletes [16]. Therefore, it has been preferred for assessing the effects of fatigue on dynamic balance [17]. To our knowledge, no study has compared the fatigue effects of different muscles on homogenous subjects. Thus, the present study aimed to assess the effects of fatigue in 5 muscle groups on the dynamic balance of healthy male volleyball players.

2. Methods
This prospective quasi-experimental study with a pretest-posttest design was conducted at a Sports Center affiliated with the university. All study protocols (balance assessment and fatigue induction) were approved by the Ethics Committee of the relevant university. A written informed consent form was received from all study participants.
Fifteen healthy professional male volleyball players (Mean±SD age: 22.0±3.4 years; height: 181.1±4.1 cm; weight: 74.4±5.2 kg) were selected by convenience nonprobability sampling method to participate in the present study. They practiced volleyball 3 times a week for a minimum of 2 years. They presented no history of lower extremity pathology or balance disorders in the previous year. All stages of the test were performed on all individuals at a specific time of the day (about 10:00 AM) to prevent daytime influences on balance and to control the variability of fatigue on the different days. Moreover, the research participants were requested to only perform their usual activities between the assessment days. 
The SEBT was used as a dynamic balance test with high reliability and feasibility [16, 18]. The SEBT was performed before and immediately after inducing fatigue in 5 lower extremity muscles; knee extensors and flexors, hip abductors and adductors, and ankle PFs.
The dominant leg was considered as the support leg on the center of the star. It was determined as the leg by which the study participant preferred to kick a ball. Each study participant performed the test 3 times for familiarization. Those with dominant right limb and left limb accomplished the test counterclockwise and clockwise, respectively.
Each study participant stood on his dominant leg at the center of the star and performed the reach action using the other leg without error in each vector of the star. Reach distance was recorded by measuring the distance between the contact point of the free leg and the center of the star. The research participant performed the test 3 times per direction. The average value of these repetitions was calculated and divided by the limb length. Then, the value was multiplied by 100 to obtain the distance as a percentage of limb length per direction [19]. For measuring the composite reach distance score, the average value of the reach distance in 8 directions was calculated [20]. In total, 6 evaluation sessions were conducted for each study participant. In the first session, the only familiarity with the test was performed.
An ankle PF machine, a knee extensor, and a flexor machine, as well as a hip abductor and adductor machine, were applied to induce muscular fatigue. Initially, the research participant was requested to complete a 5-minute warm-up. Then, the Maximum Voluntary Contraction (MVC) of the knee extensor muscles was measured by a dynamometer (Lafayette, USA.116). Accordingly, the study participant was requested to extend his knee as strongly as possible for 5 seconds. This action was repeated two times more; subsequently, the maximum value was considered as the MVC for the knee extensors. The MVC for the knee flexors, ankle PFs, hip abductors, and adductors were measured, similarly.
Next, the explored athlete was requested to perform one set, including 50 repetitions of knee extension using 50% of 1 Repetition Maximum (RM) by the knee extension machine (Figure 1). If the study subject was unable to complete 50 knee extension movements, the MVC was re-measured by the dynamometer. If the MVC was reduced to 50%, fatigue was confirmed. However, if after 50 extension movements the study participant could continue the movements, a 4-minute break was given to him. Then, he was requested to repeat the knee extension movements like the first stage and the dynamometer was used for measuring the MVC [21].
Fatigue in other muscles was induced similarly with a 72-hour interval between each muscle group test [22].
Statistical analyses were performed using SPSS v 22. Kolmogorov-Smirnov test was applied to determine the normality of the collected data. The mean composite reaching scores of the SEBT as well as mean reaching scores per common direction (anterior, posteromedial, posterolateral) were compared before and after fatigue induction in the 5 muscle groups (ankle PF, knee extensor, knee flexor, hip abductor, & hip adductor muscles) by a one-way repeated-measures Analysis of Variance (ANOVA). Mauchly’s Test of Sphericity data indicated that the assumption of sphericity had been violated P<0.05; therefore, a Greenhouse-Geisser correction was performed. Bonferroni test was also used as a post-hoc examination. Effect sizes and Partial Eta-squared are reported by . The significance level was set at 0.05.

3. Results
Fifteen healthy professional male volleyball athletes with the Mean±SD age of 22±3.4 years were tested before and after fatigue induced in the 5 muscle groups by the SEBT. Before fatigue induction, the minimum and maximum of the reach distance, for the average of 8 directions were measured as 84cm and 95.1cm, respectively (Table1). 

For composite reach scores, we achieved a result of F2.8, 39.18=23.23, P=0.0001, ղ2=0.62) Repeated-measures ANOVA results indicated the significant effects of fatigue on the composite reach score of the SEBT (Graph 1). Bonferroni post-hoc test data revealed that the fatigue of all muscle groups significantly decreased the mean value of composite reach, compared to the pre-fatigue conditions (Table 2). 

In the anterior direction, repeated-measures ANOVA findings demonstrated that fatigue in 5 muscle groups significantly impacted the SEBT score (F2.53, 35.4=38.55, P=0.0001, ղ2=0.73) (Figure 2).

Post-test results signified that the fatigue of all muscle groups significantly decreased the mean distances in the anterior direction, compared to the pre-fatigue conditions (Table 2). 
In the posteromedial direction; fatigue in 5 muscle groups significantly affected the SEBT score (F2.43, 34.1=3.11, P=0.048, ƞ2=0.18) (Figure 2). Bonferroni post-hoc test data demonstrated that only the fatigue of knee extensor and ankle PF muscle groups significantly decreased the mean distances in posteromedial direction, compared to the pre-fatigue conditions (Table 2). 
In posterolateral direction, fatigue in 5 muscle groups significantly influenced the SEBT score (F2.79, 38.99=5.52, P=0.004, ƞ2=0.28) (Figure 2). Bonferroni post-hoc test results indicated that only the fatigue of knee extensor (P=0.006), hip abductor (P=0.011), hip adductor (P=0.006), and ankle PF (P=0.005) muscle groups significantly decreased the mean distances, compared to the pre-fatigue conditions (Table 2).

4. Discussion
The present study assessed the effects of lower extremity muscle fatigue on dynamic balance in healthy male volleyball players. We also examined the potential differences between these effects. The relevant results indicated that fatigue in the ankle PFs, knee extensors, and flexors, hip abductors and adductors, decreased the composite reach score of the SEBT. Additionally, we found no difference between the effects of fatigue in various muscle groups on the SEBT. Furthermore, all muscles presented similar negative effects on reaching distance in the anterior direction. In the posteromedial direction, only knee extensors and ankle PFs decreased the reach. In posterolateral direction, the fatigue of all muscles decreased the reaching distance, except for the knee flexors. 
Literature about the effects of lower extremity muscle fatigue on dynamic balance is sporadic; thus, it is impossible to make a proper judgment to compare the effects of major muscle groups on volleyball players’ balance. This is especially true when these are evaluated by the SEBT as a sports-specific inventory.
In agreement with our results, Abdolvahabi et al. [21]found a significant decrease in all 8 directions following the fatigue of ankle PFs and knee extensors in the elderly. Vuillerme et al. [7] also found balance disturbance following the fatigue of calf muscles in healthy students. 
In contrast to our findings, Joudeh et al. [23] reported that fatigue of PFs and knee extensors reflected no influence on the balance of the healthy male population. However, the fatigue-inducing protocol and the outcome measure of our study were different from that study. We used the SEBT which evaluates dynamic balance and can predict lower extremity injury.
Regarding the fatigue effect on reaching scores in anterior and posterior directions, Abdolvahabi et al. suggested a further decrease for knee extensors, compared to ankle PFs [21]. This is inconsistent with our findings, where knee extensors and PFs presented similar effects in all directions. This may be due to the different populations and genders used in these investigations. Knee extensors and ankle PFs are more active than other muscles, especially during jumping and landing in volleyball [24]. Evaluating the composite and 3 main directions scores highlights that knee extensors and ankle PFs’ fatigue provide more prominent effects on balance than the other muscles. 
These findings suggest that the effects of muscular fatigue on the dynamic balance may be different according to the direction, i.e., tested or the fatigued muscle group. Thus, it may be better to increase the knee extensors’ and ankle PFs’ strength in the volleyball players. This is especially true when the goal is preventing fatigue and improving functional performance in the late stages of rehabilitation.

5. Conclusion
According to our results, regarding composite reach distance, the fatigue of ankle, knee, and hip muscles similarly decreased dynamic balance. However, evaluating 3 main directions revealed that knee extensors and ankle PFs fatigue present more prominent effects on volleyball players’ balance than the other muscles.

Ethical Considerations
Compliance with ethical guidelines
The current study was approved by the Ethics Committee of the Tehran University of Medical Sciences. All study participants signed a written informed consent form.

Funding
This study was supported by the Tehran University of Medical Sciences. 

Authors' contributions
Study concept and Methodology: Mohsen Bayat, Nastaran Ghotbi, Kazem Malmir; Data collection: Mohsen Bayat; Analysis and interpretation of data: Shohreh Jalaei, Nastaran Ghotbi; Writing – original draft: Mohsen Bayat, Nastaran Ghotbi, Kazem Malmir, Shohreh Jalaei; Writing – review & editing: Nastaran Ghotbi, Shohreh Jalaei; Supervision: Nastaran Ghotbi.

Conflict of interest
The authors declared no conflicts of interest.

Acknowledgments
This study was supported and approved by the Tehran University of Medical Sciences. 


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