Recovery has recently been recognized to be as important to athletes as the physical training regimen itself. The degree of recovery directly affects the following performance, and the likelihood and potential for injury. In particular, a critical issue for both athletes and their coaches is the ability to recover from local muscle fatigue and the impact of that fatigue on subsequent performance. Local muscle fatigue is the most commonly encountered form of fatigue, both daily and in training and competitions.
Local muscle fatigue represents a complex phenomenon that encompasses various factors: structural and energetic changes in local muscle tissue, and changes in activity level and the efficiency of the nervous system (6). Therefore, muscle fatigue is also referred to as neuromuscular fatigue and is divided into 3 headings based on the location of where the fatigue is induced: central fatigue, fatigue of the neuromuscular junction, and muscle tissue fatigue (5,21). Furthermore, muscle fatigue is often conveniently divided into just 2 categories:
- 1. Central fatigue, which encompasses all of the supraspinal and spinal physiological phenomena resulting in a decrease in motoneuron excitation.
- 2. Peripheral fatigue, which indicates a decrease in the contractile strength via changes in the structure and the metabolism of muscle tissue and includes the fatigue at the neuromuscular junction (5,10).
When both forms of fatigue are fully treated and the fatigue is eliminated, then local muscle fatigue is theoretically fully healed. However, the reality is that the most common techniques for recovery, such as hydrotherapy or soft tissue massage, focus on peripheral fatigue because it is considered to have a greater impact on muscle fatigue than central fatigue.
The condition widely reported as a major cause of peripheral fatigue is exercise-induced metabolic acidosis in the muscle tissue (3,5,13,32). Metabolic acidosis is caused by the intracellular concentrations of proton (H+) and inorganic phosphate (Pi), which are created by the activity of the anaerobic metabolic pathways and result in a decrease in blood pH (3,5,13,29). During the process of cellular acidosis, increased lactate production occurs and prevents pyruvate accumulation (29), and thus, blood lactate concentration is a good indirect marker of muscle metabolic acidosis levels. A sufficient supply of oxygen enhances the removal of the metabolites by activating the mitochondria, which consumes H+ and Pi as substrates for mitochondrial respiration during recovery (3,5,32). Such metabolic products are greatly induced under the condition of oxygen debt with the activity of anaerobic metabolic pathways, and thus, oxygen supplementation is easily imagined to accelerate the improvement of such acidotic condition. Given this, the use of supplemental oxygen would enhance metabolic acidosis recovery, and thus, peripheral muscle fatigue would reduce quicker than without the use of oxygen supplementation.
Within the field of sports sciences, the use of hyperoxia exposure is an ongoing research modality and the reported effects are both conflicting and complicated. The conflicting nature of the reported effects in turn makes the formulation of appropriate application regimens problematic. The following examples show this complexity and uncertainty in the findings: Hyperoxia applied during recovery sessions between intensive intermittent exercises (30% O2 gas breathing for a total of 18 minutes) was reported to be effective in removing the lactate accumulation (19); however, another hyperoxia strategy (100% O2 gas breathing, for a total of 30 minutes) did not show to have such an influence on blood lactate (31). Furthermore, a similar recovery strategy using hyperoxic gas (99.5% O2 for 20 minutes in total) in well-trained populations showed that the perception of recovery of the participants were significantly improved when compared with the control group (25), whereas other uses of oxygen gas (40% O2 for 29 minutes in total, and 99.5% O2 for 10 minutes in total) concluded that there was no effect on the rate of perceived exertion (22,24). Given this complexity, the precise nature of the effect that supplemental oxygen would have on performance, fatigue, and recovery conditions remains unclear. Additionally, studies to date have seldom considered the use of exposure to normobaric hyperoxia as a method of oxygen supplementation, and thus, an understanding of how recovery protocols under normobaric hyperoxia affects acutely developed local muscle fatigue is also unclear and imprecise.
Accordingly, this study aimed to identify and establish the recovery effects resulting from repeated exposure to normobaric hyperoxia on local muscle fatigue. This study focused on local muscle fatigue in the quadriceps, and an intermittent isometric exercise was chosen as the method of inducing the fatigue. We also aimed to clarify the mechanisms of recovery resulting from hyperoxygenation of the muscle tissue, by focusing on the level of lactate concentration in the blood. It was hypothesized that the use of normobaric hyperoxia would enhance local muscle fatigue recovery as a result of improvements in the muscular acidotic conditions.
Experimental Approach to the Problem
Local muscle fatigue is often defined as “any exercise-induced reduction in the maximum capacity to generate force or power output” (36), and this simply indicates the point at which an individual is unable to perform a certain task. To observe this state, pre- and posttask measurement of the maximum voluntary contraction is a general procedure and recognized “gold standard” (36). In addition, the endurance time until the task fails is also a simple and easily observed indicator of the level of fatigue. To observe the condition of metabolic acidosis, blood lactate concentration, which is a good indirect parameter of metabolism in muscle tissue, was observed. Moreover, the subject's perceived level of exertion was measured for an understanding of the subjective influences of hyperoxia and for clarification of its relationship to the metabolic acidosis. The experimental design implemented in this article was a counterbalanced repeated-measures fashion involving 2 trials.
Twelve healthy male subjects having a mean age of 20 years (range, 18–21 years) and with no self-reported cardiovascular disease, respiratory disease, or musculoskeletal disorders volunteered to participate in this study. Body height, mass, and body mass index were 170.1 ± 6.2 cm, 61.7 ± 10.6 kg, and 21.3 ± 2.6 kg·m−2, respectively. None of the subjects were competitive athletes, although all were physically active. To familiarize the subjects with the experimental protocol, all subjects participated in a rehearsal session before the actual study session. They were instructed to avoid alcohol consumption and any vigorous exercise, which might cause delayed onset muscle soreness for at least 24 hours in advance of the experiment. Written informed consent was obtained from all participants before the initiation of the study, and the protocol was approved by the Koriyama Tohto Academy Educational Foundation Ethical Committee.
During the experimental sessions, all participants performed 3 sets of 3 repetitions, with each repetition to last for no less than 30 seconds (3 × 3 × best effort ≥30 seconds) of isometric quadriceps contraction with a recovery session between each set (Figure 1). The recovery strategy was a 15-minute seated rest in an oxygen-controlled room (23) in 1 of 2 different conditions: normobaric normoxia (NOX; 20.9% O2) or normobaric hyperoxia (HOX; 30.0% O2). Upon arrival to the experimental room, subjects were required to complete a 5-minute warm-up of the right quadriceps followed by a 15-minute rest period as a stabilization period. The subsequent physical task was designed to fatigue the quadriceps of the right leg by sustaining an isometric load set at 70% of an individual's maximum voluntary isometric contraction (MVIC), which was measured in an earlier session. Participants were asked to maintain this load for as long as possible, and it was envisioned that exhaustion would be reached between 30 seconds and 120 seconds. They repeated the physical task 3 times with a 30-second break separating each attempt. All subjects were able to maintain the required 70% of MVIC in the first task of each set. However, excluding the first task, 4 of the 12 subjects were unable to maintain the required 70% of MVIC for more than 20 seconds. Consequently, they were asked to maintain the contraction as a “best effort” for at least 30 seconds. The lowest recorded MVIC was 55% at the end of the “best effort.” At the conclusion of the first set of 3 physical tasks, a 15-minute recovery period was provided before the start of a second identical set and again before a third identical set. To avoid carryover effects from each session, subjects performed these protocols on 2 separate occasions at least 5 days apart. The order of testing was randomized so that 6 participants performed NOX first and the remaining 6 participants performed HOX first. They were blinded to the oxygen concentration levels and were not informed of the hypothesis of the experiment. Subjects were instructed to maintain their daily activity levels for the duration of their involvement in the study.
Maximum Voluntary Isometric Contraction
During each protocol, the MVIC of the quadriceps femoris was measured 6 times:
- T1: Before the first set of physical tasks
- T2: After the first set of physical tasks
- T3: Before the second set of physical tasks, measured immediately after the first recovery period
- T4: After the set of second physical tasks
- T5: Before the third set of physical tasks, measured immediately after the second recovery period
- T6: After the third set of physical tasks (Figure 1).
All subjects were seated on a bench-like device (T.K.K. 5710m; Takei, Niigata, Japan) accompanied with a digital dynamometer (F340; Unipuls, Tokyo, Japan) set to measure their MVIC and test their muscle response to the fatiguing physical task. The subjects positioned their trunk and pelvis against the backrest and were secured upright by a pelvic belt. Both hands gripped handgrips by their side. The starting position was set as the right knee maintained a 45° angle from full-knee extension against an immobile leg bar. In this position, the MVIC of their knee extensors was measured 3 times for a duration of 4 seconds each, and the highest of the 3 values was recorded as the subject's MVIC. Subsequent MVIC values were then normalized based on the MVIC at T1 to see the rates of fatigue and recovery over T2–T6.
Endurance Time to Exhaustion
All subjects reached exhaustion between 30 and 120 seconds during the first physical tasks, which was set at 70% of the individual's MVIC. The muscle contracting continuances during the first physical tasks of each set were recorded as E1, E2, and E3 (Figure 1) and used as one of the measurement criteria in assessing the local muscle fatigue (37).
Blood Lactate Concentration
Blood samples were collected for lactate analysis from the subject's fingertip, and the lactate concentration was determined by a portable lactate analyzer (Lactate Pro LT-1710; Arkray KDK, Kyoto, Japan) (20). Before blood collection, the tip of finger was cleaned with an alcohol swab, and a small incision was made with a lancet. The initial drop of the blood was removed and discarded, and the second drop of blood was collected for analysis. To see the changes in blood, lactate measurements were repeated over T1–T6.
A visual analog scale (VAS) was used as a representation of perceived exertion at T1–T6. Subjects were asked to make a mark on a 10-cm-long line to express the locally perceived muscle fatigue in the right quadriceps. This scale was explained to the participants during the familiarization session and before each protocol. The marked point was then measured manually using a ruler, and the value was recorded as perceived exertion.
Data are presented as mean ± SEM. Two-way (recovery environment, i.e., [NOX] or [HOX] × time, i.e., [T1–T6] for MVIC, lactate concentration and VAS, or [E1-E3] for endurance time) analysis of variance (ANOVA) with repeated measures was used for all data gained in the present study. When significant differences were detected by 2-way ANOVA, 1-way ANOVA with repeated measures and paired t-test were additionally performed to detect significant changes from the start and any significant differences between NOX and HOX, respectively. Significant differences among mean values at p ≤ 0.05 were then detected by Tukey's post hoc test following 2-way ANOVA, and Dunnett's post hoc test following 1-way ANOVA. SPSS for Windows version 21.0 (IBM, Tokyo, Japan) was used, and the statistical significance was accepted for values of p ≤ 0.05 in all analysis.
Maximum Voluntary Isometric Contraction
Depicted in Figure 2 are the normalized MVIC for T1–T6. The recovery pattern differed significantly between NOX and HOX (F(1,5) = 3.194; p ≤ 0.05). In NOX, all values of MVIC measured after the first set of physical task (i.e., at T2–T6) were significantly lower than the base of MVIC at T1 (p ≤ 0.05). In HOX, 2 observations were made. First, postphysical task MVIC (i.e., T2, T4, and T6) had significant decreases when compared with the basal value at T1 (p < 0.01). The second observed result was that the rate of MVIC after the first and second recovery periods (i.e., at T3 and T5) recovered to 92.3 ± 3.1% and 96.6 ± 5.2%, respectively. This resulted in a significantly greater recovery rate in HOX (96.6 ± 5.2%) compared with NOX (82.5 ± 3.5%), especially at T5 (p ≤ 0.05), which was at the end of a 30-minute seated recovery period. Furthermore, the mean value in HOX at T6 continued to be higher than in NOX (80.2 ± 4.4% and 72.5 ± 2.4%, respectively), although there was no significant difference statistically (p = 0.066).
Endurance Time to Exhaustion
The sustained periods to the limit of muscle contraction at 70% MVIC did not differ either between E1, E2, and E3 or between NOX and HOX. However, the time during the second and third sets of physical task (i.e., E2 and E3) tended to be shorter in both NOX and HOX. In NOX, the duration of MVIC changed marginally from 54.6 ± 7.6 seconds at E1 to 46.1 ± 5.2 seconds at E2 and 47.1 ± 5.8 seconds at E3. As in NOX, similar small changes in the endurance time were observed in HOX: 55.0 ± 7.2 seconds at E1, 47.3 ± 4.6 seconds at E2 and 43.2 ± 3.5 seconds at E3.
Blood Lactate Concentration
Figure 3 expresses the changes in blood lactate concentrations over the period T1–T6. In both NOX and HOX conditions, blood lactate levels significantly increased at T2 (6.0 ± 1.1 mmol·L−1 and 6.1 ± 0.9 mmol·L−1, respectively NOX and HOX), T4 (5.1 ± 0.8 mmol·L−1 and 7.0 ± 1.4 mmol·L−1) and T6 (5.4 ± 0.9 mmol·L−1 and 6.6 ± 1.2 mmol·L−1) when compared with the starting level at T1 (2.4 ± 0.3 mmol·L−1 and 2.7 ± 0.4 mmol·L−1; p ≤ 0.05). Throughout the protocols, the patterns of change in lactate concentration did not show any significant difference between the 2 oxygen conditions.
Perceived exertion across T1–T6, as expressed and measured by VAS, is shown in Figure 4. Visual analog scale increased significantly over the course of the protocols in both oxygen conditions (p ≤ 0.05). There were no significant differences in perceived exertion between NOX and HOX. The VAS rate at T3 showed a significant increase only in NOX when compared with the beginning (0.2 ± 0.1 cm at T1 to 2.4 ± 0.6 cm at T3; p ≤ 0.05), but it did not occur in HOX (0.7 ± 0.3 cm at T1 to 2.2 ± 0.5 cm at T3). The final (T6) VAS values in NOX and HOX were 6.8 ± 0.7 cm and 6.7 ± 0.6 cm, respectively.
The main finding of this study is that two 15-minute seated recovery sessions under HOX conditions significantly hastened MVIC recovery in the locally fatigued quadriceps (Figure 2). However, this result was not associated with changes in other parameters (i.e., endurance time, blood lactate concentration, or the perceived exertion) between the 2 oxygen conditions.
As a result of consuming nonmitochondrial sources during intermittent anaerobic exercises, a significant amount of proton (H+) and inorganic phosphate (Pi) are accumulated, and they induce a decrease in blood pH (3,4,29). This is well documented and recognized as a major cause of peripheral fatigue, and this decrease in pH ultimately leads to a decrease in the contractile strength of muscles. Similarly, fatigue at the neuromuscular junction, such as resulting from an insufficient propagation of the action potentials and neurotransmitter depletion (16), reductions in the quantity of calcium ion (Ca2+) released by the sarcoplasmic reticulum (18), and decreases in blood flow (7,30), are also reported as factors in peripheral muscle fatigue. Additionally, lactate concentration is recognized as being a good indicator of metabolic conditions within tissue, although it is not directly attributed to metabolic acidosis in muscle tissues (4,29). However, the lactate accumulation levels in our study did not show a significant difference between NOX and HOX, and the mean value was even higher in HOX than in NOX between T4 and T6 (Figure 3). There are 2 reasons that can explain this. First, because lactate is not a dead-end waste product of glycolysis but is rather an important intermediate metabolite under the anaerobic metabolism pathway (4,11,29), the values of blood lactate concentrations might not express the exact instantaneous changes resulting from the metabolic process. Second, as the result of greater force output in HOX, it is not unexpected that more lactate was produced in HOX than in NOX. Hence, it seems reasonable to suggest that the threshold of maximum peripheral fatigue was increased in HOX, and a greater force output (i.e., recovery in MVIC) could be achieved and maintained over the course of the protocols without harmful metabolic acidosis occurring.
There are a number of investigations to date that have attempted to verify the effects of a recovery strategy using hyperoxia on blood lactate accumulation; however, the previous investigations have reported conflicting results (9,19,22,31,33). One of the reasons for these conflicting results might be because of the difference in the type of exercise used in the experiments. When the exercise was performed using a fixed workload, lactate concentrations were reported to be lower in the hyperoxic environment (19,33), whereas when the exercise was done maximally or self-paced, there were no differences in reported lactate levels between normoxia and hyperoxia (9). The findings in the present study support the previous studies that used a maximum exercise, and therefore, it is reasonable to consider that HOX favorably influenced the recovery from local muscle fatigue without increasing the concentration of blood lactate.
From the present results, it is not possible to clarify the mechanism of the enhanced recovery resulting from the hyperoxygenation in the muscle tissue; however, there are 2 main hypotheses that oxygen supplementation during recovery periods could be considered ergogenic. First, HOX applied during the subject's fatigued state could increase the total arterial oxygen content and thus the rate of oxygen diffusion from the plasma into the muscle tissue cells. A prior study that examined the effects of hyperoxia during a 15-minute hyperpnea test revealed that arterial oxygen partial pressure (PaO2) significantly increased (approximately 350 mm Hg) compared with that of the control (approximately 120 mm Hg), whereas arterial oxygen saturation (SpO2) did not show a significant difference between the conditions (35). Hemoglobin-bound oxygen acts as a reservoir because it dissociates oxygen into the plasma when the oxygen in the blood is diffused into cells, as the cells consume oxygen during cellular respiration. However, the rate of oxygen diffusion is determined primarily by the difference in PaO2 between the plasma and cells. Therefore, one might assume that the SpO2 remains at approximately 97–98% during the intermittent isometric muscle exercise recovery period, and because of the increased rate of PaO2, that post-HOX performance has a potential to be greater.
Second, hyperoxia might influence the regulation of central motor output to the activated muscle and therefore of muscle force output. This is because increases in arterial oxygen content via atmospheric hyperoxia would not only affect peripheral fatigue but also central fatigue (2,34). The increased oxygen concentration in the artery influences oxygen transportation throughout the organism (15,28); therefore, changes in performance under a hyperoxic environment may occur as a result of the mechanisms of central fatigue, which dictate the level of increases and decreases of volitional motor output into the muscle tissue. Tucker et al. (34) found that the integrated electromyographic (iEMG) activity, which is used as an indirect measure of local muscle activation, was greater during 20-km cycling time trials in hyperoxia (40% O2) than in normoxia and concluded that improved performance in hyperoxia is partly because of a centrally mediated increase of the local muscle activation. Furthermore, Peltonen et al. (26) and Amann et al. (2) found that central motor output as represented by iEMG was reduced in hypoxia (15.8% O2 and 15% O2, respectively) and hypothesized that performance capacity was controlled by central neural drive as a result of brain receptors responding to changes in peripheral muscle tissue conditions, such as the level of metabolite accumulation. This mechanism is also supported by other researchers who have suggested the teleoanticipation model as a control system for performance optimization during physical activity (17). Moreover, Gandevia (10) summarized the evidence of the central factors in fatigue in a literature review and concluded that feedback from muscle afferents on the muscle's biochemical conditions and force generation capacity is likely to diminish the activation of cortical sites. In the presence of oxygen debt and lactate accumulation, group 3 and group 4 muscle afferents, which are metaboreceptors and so are sensitive to the metabolites that are generated during muscle fatigue, continue to discharge and result in the inhibition of alpha motoneuron activity (14,38). Because increasing the oxygen supply to a musculoskeletal system activates cellular activity and promotes the metabolism of fatigue substances (12), the alpha motoneuron in HOX would be activated as a result of the inhibition of peripheral fatigue-induced decruitment of motor unit, and the generated force output would be higher.
Perceived exertion, as represented by VAS in our study, showed almost identical changes across both oxygen conditions over the course of the trials (Figure 4). Perceived exertion ratings have been shown to be strong indicators of physical fatigue and not to be influenced by central factors in fatigue (1,8). Therefore, it would be reasonable to recognize the VAS scale as a reflection of peripheral fatigue rather than central fatigue. Based on this, which is similar to the result of blood lactate concentrations, our findings on VAS would express that the levels of peripheral fatigue were similar in NOX and HOX, while the force output was significantly recovered in HOX.
To sum up, it appeared that the use of two 15-minute sets of seated recovery under HOX was effective in restoring the MVIC in local muscle fatigue that had been induced by intense intermittent exercises. Although the present results could not clarify the mechanism of MVIC restoration, there might be a complex mechanism that relates to both peripheral and central fatigue factors, and these factors are sensitive to the oxygen concentration in the air.
Hyperoxia therapy has been considered and applied in the field of sports for the purpose of healing musculoskeletal injuries, increasing performance level, and accelerating the recovery from daily training. Although the evidence is mixed, the present study showed that two 15-minute recovery sessions in HOX (30.0% O2) enhanced the restoration of MVIC and that this restoration recovery rate would be approximately 14% greater in hyperoxia than in normoxia. However, there are 2 considerations that should be noted before applying the findings in our study to practical situations and to incorporating HOX supplementation into training regimens. First, although each recovery session was set up for 15-minutes, the required time for recovery would need to be longer. The reason for this is that the rates of MVIC recovery in HOX followed the same course as those in NOX between T1 and T4, which includes the first recovery session (Figure 2). Given that the value of MVIC was significantly restored by T5, which was just after the conclusion of the second recovery session, it would be more effective for subjects to rest for greater than 30 minutes under HOX. Second, the muscle used in the present study was the quadriceps whose muscle volume corresponds to approximately 2.0–2.5 kg per lower extremity (27); thus, there should be caution when migrating this result to whole-body training and competitions. However, it is possible that a large muscle group exercise is affected in a similar way to a single muscle and consequently improved by increases in the oxygen concentration in the air. Based on these considerations, it is recommended to coaches and field practitioners to use repeated 15-minute exposures to 30.0% HOX between intense intermittent exercises as an effective recovery strategy from local muscle fatigue. By doing this, athletes would be able to recover power output by approximately 14% more than just staying within a normoxic environment for the same duration.
The authors thank all subjects for their kind corporation and all stuff in the Koriyama Institute of Health Sciences for their warm supports. The results of the present study do not constitute endorsement of the produce by the authors or the National Strength and Conditioning Association. Moreover, the authors declare no conflicts of interest.
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