In team sports, such as handball, soccer, hockey, or basketball, athletes are at an increased risk of traumatic events, especially to the lower extremity joints (13,21). Injuries often occur in noncontact situations (13,15) resulting in substantial and long-term functional impairments (35). Based on the findings of Hawkins and Fuller (13) and Pinto et al. (24), who showed that injuries in soccer and ice hockey often occur in the last minutes of each half of the game, it is suggested that the injury risk is positively associated with muscular fatigue. This hypothesis is emphasized by the results of a study by Smith and colleagues (30), who showed that among multiple risk factors, the preseason perceived fatigue was the strongest predictor of in-season injuries in ice hockey players. Other injury risk factors that have been identified through prospective studies include previous injuries (17), demographic factors (21), anatomical characteristics (16), and neuromuscular and sensorimotor impairments (25). Taking these findings into account, it might be suggested that physical fatigue reduces neuromuscular and sensorimotor control and that the occurrence of these impairments may contribute to an increased lower limb injury risk. This hypothesis is partly supported by a number of studies that have examined changes in static postural control after different fatigue protocols. Most of these studies reported a significant increase in postural sway after localized (3,20,28,31,32) or whole-body fatigue (9,19,31,33). However, the inconsistent data on fatigue-related changes in dynamic balance (11,12,22) arouse questions regarding physiological mechanisms responsible for static and dynamic postural control, and whether both outcomes may respond differently to physical fatigue. Equilibrium control during standing or under dynamic conditions involves several mechanisms of sensorimotor and neuromuscular control (2,23). Although for postural balance control during upright stance the center of body mass must be kept over the supporting base, the locomotor (dynamic) balance is a more complex task, because it involves achieving a compromise between the forward propulsion of the body and the need to maintain the lateral stability of the body (2). It has previously been shown that especially joint somatosensory information from the lower legs can play an important role in perceiving and maintaining postural sway during quiet standing (7,17). Although these factors may contribute to dynamic postural mechanism as well, the ability to maintain balance during conditions of limited stability can also be influenced by lower extremity strength (8,18) and ankle, knee, or hip range of motion (10). However, because of methodological issues in the current test standards of both balance conditions, the validity of these data can be challenged to a certain extent. First, static postural sway has often been described and is generally used to assess sensorimotor organization of balance control (8,17,23) but may not be the most appropriate measure for mechanisms responsible for regaining stability, maintaining locomotion, or the execution of flexible movement patterns. Second, dynamic measures of postural control such as the star excursion balance test (SEBT), the time-to-stabilization after jump landing, or the balance error scoring system are context- and task-specific and may not assess equal components of postural stability (6). Although these considerations exist, static and dynamic postural control tests are often equally used to explain changes in sensorimotor function under conditions of physical stress-related adaptations, such as fatigue. However, in this context, it is questionable whether both conditions provide similar information. These limitations contribute to the uncertainty regarding the presence of fatigue-induced sensorimotor changes and its clinical relevance in terms of an increased injury risk. To our knowledge, no study has previously examined the influence of fatigue on changes in both static and dynamic postural control. Clarifying the influence of fatigue on both measures may help to evaluate the practical relevance of static postural control changes for athletic performance and to understand possible fatigue-related injury mechanisms.
The purpose of this study was to examine the effect of fatigue on static postural sway and dynamic balance, as measured by the SEBT, in male team handball players. For this, 2 different fatiguing protocols were used: (a) whole-body fatigue on a treadmill and (b) localized fatigue of lower extremity muscles.
Experimental Approach to the Problem
In this study, we tested the influence of fatigue on changes in postural sway velocity during unipedal stance and SEBT maximum reach distances. Both dependent variables were used to represent either static or dynamic measures of postural control. Postural sway during upright standing on a force plate and maximum reach distances of the SEBT were measured in a fixed order before and immediately after complete exhaustion. To distinguish between the effects of a whole-body fatiguing exercise involving a large number of muscles and localized exercises only fatiguing selected muscle groups, the athletes were tested under 2 experimental conditions: (a) treadmill running for whole-body fatigue (TRF) and (b) unilateral barbell step-ups for localized muscle fatigue (LMF). Both fatigue dimensions were previously used for the detection of exhaustion-associated changes in postural control. We hypothesized that both fatigue protocols increase the center of pressure (COP) sway velocity under eyes open and eyes closed conditions and decrease the SEBT maximum reach distances. Postural control was assessed barefooted on the dominant leg before and immediately after exercise. The leg dominance was determined by asking the athletes to define their ‘take-off leg’ (the leg used to take off in a handball jump shot). A Kistler force platform (model 9260AA6, Kistler Instrumente GmbH, Germany) and Bioware software (version 4.0; Kistler Instrumente GmbH, Ostfildern, Germany) were used to measure ground reaction forces during a single-leg stance.
Nineteen male team handball players (age: 16.8 ± 0.6 years; height: 179.9 ± 6.9 cm; and mass: 73.5 ± 10.8 kg, 2 German youth handball teams, first and second divisions) participated in this study. Exclusion criteria were chronic ankle instability and any lower extremity injuries (acute or overuse) that prevented the player from participating in competition or practicing for at least 1 day in the previous 6 months. Our subjects were regularly active and currently engaged in regular summer preseason handball and structured exercise training sessions (2–3 times per week). The athletes were asked to refrain from performing physical exercise 12 hours before testing. Measurements were performed before a practice session, and the coaches supervised the testing procedure. All the participants were tested at similar times of the day (between 2 and 5 pm) and were allowed to drink while exercising to avoid dehydration. All the athletes were given detailed information on the study, and written consent was obtained. Because minors were involved, parental consent for participation was obtained by the coaches of both teams. The study was nested in a research project on fatigue-related sensorimotor changes in healthy and injured athletes, and the testing procedures were approved by the local ethics committee. The study was conducted in accordance with the Declaration of Helsinki.
For static postural sway measures, the athletes were instructed to stand as motionless as possible on a force plate for 20 seconds. The test was performed 4 times (2 times with eyes open and 2 times with eyes closed) with 10 seconds of rest between trials. The best performance (lowest sway velocity) in each condition was used for data analysis. Failed attempts (lifting hands off iliac crests, stepping, stumbling, falling, lifting the forefoot or heel, opening eyes) were excluded from data extraction.
The SEBT was performed according to the method described by Gribble et al. (11). The athlete stood with the hands on the hips on the dominant leg in the center of a grid (8 lines extending at 45° increments from the center) placed on the floor. A considerable redundancy in the 8 directions was shown by Hertel et al. (15). Therefore, we used 4 (anterior, posterior, medial, and lateral) of the original 8 reaching directions to complete postfatigue measures in an appropriate time. The order of excursions was counterbalanced. Each participant completed a 5-minute test trial before baseline measurements. The athletes were asked to reach the nondominant leg as far as possible in each of the 4 directions, touch lightly on the line, and return to a double-leg stance in the center. Measurements for each direction were carried out twice before and twice after fatigue (the best performance was retained). The reached maximum distance (centimeters) from the center of the grid was manually recorded by the examiner for each direction. Foot position was marked with a tape on a removable, nonslip circular mat placed in the center of the grid. If athletes lost their balance and touched the floor with the nondominant limb before reaching the start position or lifted their hands off their iliac crests, the trial was discarded and repeated. To avoid recovery processes after fatigue, the whole postfatigue test procedure took not >4 minutes.
Whole-body fatigue (TRF) was induced by running on a motorized treadmill (h/p cosmos, Germany) with increasing speed at a constant grade of 1.5%. During the first stage of the test (minutes 1–3), the initial treadmill speed was set at 5 km·h−1. At the start of the fourth minute, the speed was set at 8 km·h−1 and increased every third minute by 2 km·h−1. The treadmill test continued until subjective exhaustion. Exhaustion was assessed immediately after the completion of the treadmill test by using the Borg 6–20 rating of perceived exertion (RPE) scale (4).
Localized muscle fatigue was induced using 3 sets of single-leg ‘barbell step-ups’ on a bench (30-cm height) with subsequent heel raises and 1-minute rest between sets. All the participants were familiar with the barbell step-up technique. The athletes completed a 2-minute test trial without weights on the barbell and were asked to define the weight appropriate for a maximum of 20–30 repetitions. If the desired number of repetitions was achieved in the first set, the weight was kept constant for the following trials. Otherwise (in 3 cases), weights were corrected by adding or subtracting weight plates. The Borg 6-20 scale was used to estimate the degree of fatigue. Each athlete started in a double-leg stance in front of the bench with a barbell across the shoulders and was asked to step up onto the bench with the dominant leg until the hip and the knee were fully extended. On the bench, the athlete performed a heel raise with the dominant leg before stepping down with the nondominant leg. The step-ups continued until the athlete was unable to perform a step-up and heel raise throughout the full range of motion. All the participants were verbally encouraged by the investigators to ensure complete exhaustion.
‘Bioware’ software (Kistler, version 184.108.40.206) was used to acquire data of force plate output at a sampling rate of 1,000 Hz. Force data were low-pass filtered at 10 Hz using a second-order Butterworth filter. The outcomes of interest were COP velocity during unipedal stance and maximum reach distance of the SEBT. The COP velocity (centimeters per second) was defined as the sum of the cumulated COP displacement divided by the total time (26). Measures of SEBT reach distances were normalized for leg length (11).
For statistical analyses of fatigue-related changes in both dependent variables, a 2 factorial linear mixed model (SEBT) and a 3 factorial linear mixed model (COP), appropriate for repeated measures data, were specified for each of the main outcomes. The experimental factors ‘fatigue,’ ‘protocol,’ and ‘eyes condition’ were included as fixed factors nested in the individual's factor. Static sway velocity and mean SEBT reach distance were defined as dependent variables and analyzed separately in stepwise linear regression models. To allow for random individual variability, a random intercept model (14) was used and an unstructured variance covariance matrix was assumed. Effects are presented as nonstandardized effects estimated from β coefficients in the linear mixed effects model. Relationships between static and dynamic postural control changes (baseline vs. postfatigue differences) were analyzed using Pearson product-moment correlations. The level of statistical significance was p ≤ 0.05. The sample size for the study was based on power calculations to detect fatigue-induced differences with an effect size of 0.25, a power of 80%, and a significance level of 0.05. Test-retest reliability between prefatigue values was calculated with the intraclass correlation coefficient (ICC) and the standard error of measurement (SEM). All statistical analyses were performed by a statistician using the statistical software R.
The mean RPE was 17.2 ± 1.3 after treadmill running (TRF) and 18.9 ± 0.7 after the LMF protocol. At baseline, there were no differences in the COP velocity and SEBT mean maximum reach between both fatigue protocols. The ICC between the baseline values of both tests was moderate (COP velocity eyes open = 0.605, confidence interval [CI] −0.090, 0.857; COP velocity eyes closed = 0.761, CI 0.356, 0.913; SEBT = 0.860,CI 0.623, 0.949). The SEM was at 9.0% for COP velocity eyes open, 6.8% for COP velocity eyes closed, and 1.1% for SEBT maximum reach.
The COP velocity increased after both fatigue protocols under eyes open (TRF: 47 ± 68%; LMF: 10 ± 30%) and eyes closed (TRF: 10 ± 11%; LMF: 11 ± 20%) conditions (Table 1). A main effect was shown for fatigue (p < 0.05) and eyes condition (p < 0.01), whereas no effect was found for the protocol (Table 2). No differences in changes over time and eyes condition were present for TRF and LMF, respectively.
No effects were observed for the SEBT (Table 3). There were no significant correlations between the relative change in the COP velocity with eyes open (TRF: r = −0.25; LMF: r = 0.18) or eyes closed (TRF: r = 0.22; LMF: r = 0.02) and the relative change in SEBT mean values.
In this study, static postural control during upright standing was negatively affected by 2 different fatigue conditions, whereas the SEBT reach distances remained unchanged. There were no significant differences in the effects of the 2 fatigue protocols, suggesting that running and peripheral lower limb exercises contribute similarly to changes in neuromuscular and sensorimotor mechanisms accountable for upright standing stability. Fatigue-related impairments in postural control during quiet standing have previously been shown by a number of researchers. They reported a significant increase in sway velocity (3,20) and horizontal or sagittal sway (9,31,33) after whole-body and LMF in young and physically active people. Regarding changes in static postural sway, our data also show no statistical differences between both eyes conditions. This suggests that the visual feedback has little impact on fatigue-related sensorimotor changes. In fatigued and unfatigued conditions on the other hand, the postural sway velocity was significantly greater when visual feedback was withdrawn. The compensatory influence of visual feedback on the perceived postural sway during single-leg stance has been reported by Fitzpatrick and McCloskey (7).
Although static postural sway has been described as an appropriate measure for sensorimotor control (23), the use of quiet standing on a force plate may be of limited value for the detection of underlying injury mechanisms. Postural control during locomotion is often associated with reactive, compensatory movements after random external disturbances that are applied either directly to the subject or to the support on which the subject is standing or walking (2). Because such conditions occur frequently in team sports, and are often associated with lower extremity injuries (1), dynamic postural control measurements may provide a broader approach to understand injury-associated sensorimotor control mechanisms. In this study, we used the SEBT to assess dynamic balance. Lower SEBT reach distances have been shown to be associated with an increased lower limb injury risk (25) and knee flexibility (27). It is also suggested that neuromuscular coordination and strength may influence the SEBT performance (25). Furthermore, studies (11,25) reported lower SEBT reach distances after lower limb injuries, which might be a result of posttraumatic or postoperative sensorimotor impairments. In our study, the maximum SEBT reach distances remained unchanged after both fatigue protocols. Thus, it could be suggested that although fatigue affects static postural control, sensorimotor mechanisms responsible for regaining dynamic balance in healthy athletes remain predominantly intact. However, multiple test paradigms exist to assess dynamic balance and it is questionable whether the results of single tests can be used for general statements. It is likely that the variety of assessment methods is partly responsible for the diversity in reported findings regarding fatigue-related changes in dynamic balance. Gribble et al. (10–12) investigated the effects of fatigue on the SEBT in noninjured adults and patients with chronic ankle instability. In contrast to our findings, they reported a significant decrease in all reach directions after lower extremity muscle fatigue in healthy participants (12). Other studies showed different effects (significant increase or decrease or no change) of fatigue on dynamic balance abilities, using jump-stabilization measures or balance time on unstable surfaces (22,29,34). The diversity between these findings emphasizes the need of a gold standard assessment for the detection of sensorimotor control changes during unstable postural conditions.
There are some methodological limitations that may influence the conclusions that can be drawn from this study. Both postural tests were conducted in a fixed order, and thus, it is likely that the fatigue-induced changes of the second test (SEBT) might have been diminished to a certain extent. However, in a previous study, it has been shown that postural control is significantly affected until 8 minutes postfatigue (20). In this study, the SEBT started 2 minutes after the completion of the fatiguing exercise, and no participant took >4 minutes for the whole postfatigue test procedure. It therefore seems likely that potential fatigue effects on the SEBT, even if diminished, would have been detected in this study. Other limitations concern the uncertainty regarding the use of adequate fatigue protocols. In this study, the athletes performed single-leg barbell step-ups with subsequent heel raises and treadmill running to induce physical fatigue. Although the barbell step-up movement activates more muscle groups than the single-leg heel raise does, the exercise is considered as appropriate for a localized fatigue protocol (5). Regarding the treadmill protocol it appears problematic that the running movement does not strictly differentiate between general (and therefore more cardiovascular) and LMF and that both factors may contribute to changes in postural control. However, no differences were found between both protocols in fatigue-related changes in static or dynamic balance. In contrast to our findings, Springer and Pincivero (31) reported significant differences in fatigue-induced changes between whole-body and LMF. The inconsistencies may be explained with differences in participants or fatigue protocols. Although Springer and Pincivero (31) examined healthy subjects of both sexes without a clear definition of the activity background, this study included healthy male youth handball players. Therefore, it might be possible that either the performance status or gender differences were responsible for the inconsistent results.
In conclusion, our data support the findings of previous research on the fatigue-related impairments in static postural control. Because of the lack of prefatigue vs. postfatigue differences in SEBT reach distances, the role of sensorimotor control in unstable situations during sports-related exhaustion (such as direction changes, side-cutting, and jump-landing movements) remains unclear. Therefore, conclusive statements regarding the influence of fatigue on dynamic postural control are premature without fully understanding the details and control mechanisms of different dynamic balance tasks.
Static sway velocity in male team handball players was influenced by whole-body and LMF. This suggests that both fatigue dimensions change neuromuscular and sensorimotor control mechanisms during upright standing and may increase the injury risk in team athletes. Contrary results were obtained for the SEBT. Both the treadmill fatigue protocol and the LMF protocol resulted in no changes in maximum reach distances. This implies that physical fatigue does not result in major alterations in sensorimotor control mechanisms responsible for dynamic balance in healthy athletes. Thus, our data indicate that the exclusive use of static postural sway does not necessarily lead to conclusive findings and that future assessments on injury risk–related sensorimotor impairments should include dynamic balance tests such as the SEBT. However, because it is questionable whether the SEBT is the most appropriate dynamic postural control assessment, it would be helpful for future studies to compare the fatigue-related effects on sports-specific sensorimotor control by using different measures of dynamic balance.
Financial Disclosure & Conflict of Interest Statement: The research reported in our article was not supported by funding from any outside agency or group. No commercial party has a direct financial interest in the results of the research.
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