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Original Research

Effects of Hyperbaric Oxygen on Muscle Fatigue After Maximal Intermittent Plantar Flexion Exercise

Shimoda, Manabu1; Enomoto, Mitsuhiro1; Horie, Masaki1,2; Miyakawa, Shumpei3; Yagishita, Kazuyoshi1,4

Author Information
Journal of Strength and Conditioning Research: June 2015 - Volume 29 - Issue 6 - p 1648-1656
doi: 10.1519/JSC.0000000000000809
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Abstract

Introduction

Hyperbaric oxygen (HBO) treatment is a minimal invasive treatment that delivers 100% oxygen under increased pressure. Such treatment increases the levels of dissolved oxygen in the blood and subsequently causes high partial pressure of oxygen in the peripheral tissue, thereby exerting beneficial effects on conditions related to a low O2 environment, such as carbon monoxide poisoning, decompression sickness, arterial gas embolism, tissue oxygen depletion due to radiation-induced tissue injury (28), and skin ulcer attributed to peripheral circulatory failure. In sports injuries, soft tissues, including muscle, ligament, and tendon, are often damaged as the result of oxygen depletion due to edema or bleeding in the injured tissue. Therefore, HBO treatment may be beneficial for healing ligamentous injury of knee or ankle, joint sprain, or muscle injury (25).

In previous studies, HBO treatment enhanced the recovery of eccentric torque of the quadriceps muscle from delayed onset of muscle soreness caused by eccentric contractions of the muscle (26) and accelerated the recovery of plantar flexion peak isomeric torque, pain sensation, and unpleasantness in exercise-induced muscle damage caused by eccentric contractions of the gastrocnemius muscle (29). These findings suggest that HBO treatment is effective for enhancing recovery of decreased muscle force induced by exercise. However, it was reported that recovery from delayed onset of muscle soreness caused by eccentric contractions of the elbow flexor muscle group (17,21) and knee flexor muscle group (6) did not differ between subjects receiving HBO treatment and those not receiving it. Those different results of HBO effects may be attributed to magnitude of the injury, reduction in the inflammatory processes after injury, or oxygen diffusion gradient for optimal healing (17). The degree of muscle damage induced by a type of exercise would be important for the differences. Thus, the effect of HBO treatment on the recovery of decreased muscle force remains controversial.

Of the many combinations of factors involved in exercise-induced decreases in muscle force, we focused on muscle fatigue. Muscle fatigue can describe the gradual decrease in the force capacity of muscle or the end point of a sustained activity (11). Possible reasons for muscle fatigue include a failure of the central nervous system to excite the motor neurons adequately and decreased voluntary activation due to factors such as impairment of neuromuscular propagation (1,5,13). It was further reported that the time to exhaustion was shorter and the rate of leg maximal voluntary contraction (MVC) fall was greater for hypobaria than normoxia during knee extension exercise (14). Conversely, inspiration of hyperoxic gas increases the time to exhaustion; in other words, it delays the progression of exhaustion (18). These results suggest that muscle oxygen uptake influences the decline in the force capacity of muscle and that hyperoxia and HBO affect the endurance of muscle force.

The aim of this study was to investigate the effects of HBO treatment on muscle force and muscle activation during endurance exercise to reveal the impact of prior HBO on fatiguing contractions and muscle activation. We hypothesized that HBO treatment enhances the endurance of muscle activation, thereby enhancing the endurance of muscle force.

Methods

Experimental Approach to the Problem

Subjects performed fatiguing isometric plantar flexion exercise and underwent electrical stimulation of the dominant calf on a Cybex 6000 isokinetic dynamometer (Lumex, Inc., New York, NY, USA). We compared the torque, amplitude, and frequency of electromyography (EMG) in the triceps surae muscle during fatiguing isomeric plantar flexion exercise between subjects who received HBO and those who received normoxic treatment. We also measured the torque and EMG during MVC and the torque, EMG and evoked compound action potential (M wave) in response to electrical stimuli to elucidate the muscle activation before and after intervention.

Subjects

Twenty healthy males (aged from 21 to 24 years) volunteered to participate. The subjects were physically fit and had never injured the ankle joint or plantar flexor muscle groups. They were also instructed to refrain from specific resistance training of the plantar flexor muscle groups 12 hours before the experiment, but no restrictions were placed on hydration, diet, or medication. The experimental protocol involved a randomized single-blind design. The subjects were randomly assigned to an HBO or normoxic group and were blinded to their treatment and group assignment. The average age, height, and body mass of the subjects were 22.0 ± 1.1 years, 170.9 ± 7.6 cm, and 64.8 ± 7.4 kg in HBO group, and 21.9 ± 0.7 years, 174.2 ± 4.6 cm, and 65.4 ± 7.2 kg (mean ± SD) in normoxic group. There were no significant differences between the groups.

Approval for this study was obtained from the Ethics Committee of Tokyo Medical and Dental University. All subjects were fully informed of the study procedures and signed an informed consent form indicating that they understood the study procedures and the risks and benefits of participation.

Procedures

The time course design of this study is shown in Figure 1. The protocol for tests 1, 2, 3, and 4 remained the same and involve MVC and twitch interpolation test, and fatigue test (FT) before intervention between test 1 and test 2 and FT after intervention between test 3 and test 4 were performed. The subjects underwent HBO or normoxia treatment between test 2 and test 3. The subjects performed a practice in 1 day of a week before the experiment to familiarize with the protocol. The protocols of twitch interpolation test and FT of this study were referred from Nordlund et al. (22) and Taylor et al. (27).

Figure 1
Figure 1:
An experimental protocol of this study. Maximal voluntary unilateral isometric plantar flexions were performed 50 times as an FT before and after intervention. MVC and twitch interpolation tests were also performed before and after FT, indicating as test 1 to 4. The subjects were randomly assigned to an HBO or normoxic group. FT = fatigue test; MVC = maximal voluntary contraction; HBO = hyperbaric oxygen.

The ankle joint was set in a position where the foot was 0 degrees of plantar flexion. Subjects lay prone on a test bench with the dominant leg fully extended and the dominant foot placed on a Cybex footplate, secured tightly with hook and loop straps. Subjects were also secured with straps around the hips and right thigh to minimize excessive body motion. The dynamometer was aligned to the center of the ankle joint and the lever arm length was measured.

Surface Electromyography and Torque Recording

The EMG of the triceps surae muscles was recorded from the soleus and medial and lateral gastrocnemius muscles (MG and LG, respectively) of the dominant calf through surface electrodes attached to amplifiers. Surface electrodes with a diameter of 5 mm were placed at interelectrode distances of 30 mm in a bipolar electrode configuration on the respective belly of each muscle. The active electrode was placed over the motor point on the middle of the muscle belly, and the reference electrode was placed over an electrically neutral site over the femur epicondyle.

The torque and EMG signals were recorded through a PowerLab 8/35 analog-to-digital converter (PL3508; AD Instruments, Colorado Springs, CO, USA) at a sampling rate of 1 kHz. The EMG signals from the soleus, MG, and LG corresponding to each muscle contraction during the FTs and the pre- and post-exercise MVC and twitch interpolation tests were recorded. Electromyographic signals were amplified with a bandwidth frequency of 10–2000 Hz (rejection ratio >80 dB; input impedance, 100 MΩ).

Twitch Interpolation Test

An evoked potential-measuring instrument Neuropack μ (MEB-9102; Nihon Koden, Tokyo, Japan) was used to electrically stimulate the tibial nerve and obtain the evoked twitch torque of the triceps surae muscles. The stimulating electrode, with a diameter of 2.5 cm, were placed on the skin of the popliteal fossa of the dominant leg and oriented parallel to the estimated path of the tibial nerve with distal placement of the anode. Once positioned correctly, subjects briefly warmed up with submaximal plantar flexions, a single stimulus was used to obtain the M wave. The stimulus that produced maximum motor response was determined by progressively increasing the intensity until the torque and the M wave plateaued. The level of stimulation was then set at 10–20% above this point. The M wave, which was induced by the single stimulus, was also recorded, and the peak-to-peak amplitude and duration were determined. The single stimulus was performed first followed by 2 MVCs of the triceps surae separated by 30 seconds. Two MVCs were performed for 3 seconds each. We used triple stimuli (interstimulus interval, 10 ms) to determine activation of the triceps surae during MVC with a superimposed twitch technique (22,27). The activation of the triceps surae during MVC was calculated as activation (%) = [1 − superimposed twitch torque during MVC/control twitch torque] × 100. The control twitch torque in response to each stimulus was analyzed. To study the changes in the contractile properties of the involved muscles, the contraction time taken from stimulation to peak twitch torque and half relaxation time taken for the twitch torque to decay by one-half were analyzed for all control twitches.

Fatigue Test

After the MVC test followed by a sufficient rest period (3 minutes), all subjects in both groups performed maximal isometric plantar flexion intermittently, that is, a 2-second contraction followed by a 2-second rest repeated 50 times. Strong verbal encouragement was given during all contractions to help elicit a maximal effort contraction. In addition, the torque output including MVC and FT of each subject were continuously displayed on a computer screen to display his achievement throughout the test. All subjects performed 2 FTs before and after intervention (HBO or normoxic). The times between the end of intervention and the beginning of the FT after intervention were 23 ± 5.4 minutes in HBO group and 22.5 ± 5.4 minutes in normoxic group.

Electromyographic electrodes were placed on the muscles at the beginning of the experiment and left in place until completion of the experiment. Subjects refrained from touching the electrodes while receiving specific treatment. To ensure low levels of movement artifacts, electrode cables were fastened to the subjects' triceps muscles with medical adhesive tape. The averaged torque over 1 second during voluntary contraction except during the increase and decrease phases was adopted as MVC torque.

Data Analysis

During voluntary contractions, the root mean square (RMS) amplitude of EMG was calculated over a 1-second period. For the EMG power spectrum, fast Fourier transformations were used to obtain the mean power frequency (MPF). The window length was set at 1024 data points during voluntary contraction according to the method of Amann et al. (3). As the EMG amplitude of the first 3 contractions was lower than that of the later contractions in most of the subjects, EMG and torque data in the first three of fifty contractions were not used. Although the subjects practiced the maximal planter flexion previously, they could not exert the highest torque at the first contraction due to inexperience of the maximal planter flexion. The torque and RMS and MPF of EMG (average of 1 second during contraction) were pooled for contractions 4–10, 11–20, 21–30, 31–40, and 41–50, respectively. The percentages of declines of the torque and RMS and MPF values in contractions 11–20, 21–30, 31–40, and 41–50 were calculated for the initial value of 7 contractions (averaged value of contractions 4–10) during the FT.

Hyperbaric Oxygen and Normoxic Treatments

Before entering the hyperbaric chamber, subjects were examined by a doctor to ensure that they had no contraindications to hyperbaric treatment. The HBO and normoxic treatments were performed in a multiperson hyperbaric chamber (NHC-412-A; Nakamura Tekkosyo, Ibaraki, Japan) under the supervision of trained medical personnel at the Tokyo Medical and Dental University Hospital. The gas supply to the chamber was covered with drapes to ensure that subjects were blinded to their treatment.

For the HBO treatment, subjects were compressed to 2.5 ATA over 15 minutes, after which they breathed 100% oxygen for 60 minutes delivered through a tight-fitting mask covering the nose and mouth for three 20-minute periods with 5-minute breaks in ambient air (20.9% oxygen). Two 5-minute air breaks in ambient air were carried out in 2.5 ATA. At the end of the 60-minute period, 15 minutes were allowed to decompress to atmospheric pressure. The treatment table for this study requires a 5-minute air break every 20-minute oxygen inhalation, to avoid oxygen toxicity. For the normoxic treatment, subjects were compressed to 1.2 ATA and breathed room air for 70 minutes. This pressure was sufficient to ensure that subjects experienced the symptoms of external pressure changes, but it did not result in a marked increase in oxygen tension. Both treatments were administered to each subject within 1 hour after the first MVC and electrical stimulation and FTs. Each subject received 1 treatment.

Statistical Analyses

Data are expressed as mean ± SE except for age, height, and body mass of the subjects. The difference on the FT results between the HBO and normoxic treatments was analyzed by 2-way analysis of variance with repeated measures. When significance was found, the unpaired t-test was used for post hoc analysis to determine the difference between the HBO and normoxic treatments. The unpaired t-test was also used to determine the significance of the differences on the MVC and electrical stimulation test (tests 1–4) results between the HBO and normoxic treatments. Significance was set at P ≤ 0.05 in all analyses.

Results

Voluntary Plantar Flexion Torque During the Fatigue Test

Torque during repetitions 41–50 in the FT decreased to 82.5 ± 6.2% and 79.7 ± 2.1% of the initial values during repetitions 4–10 before HBO and normoxic treatment, respectively, and 88.5 ± 1.8% and 83.2 ± 1.9% after HBO and normoxic treatment, respectively. The declines in torque were significantly different between the groups and dependent on the number of repetitions. Torque levels were continuously higher throughout the test in the HBO group than in the normoxic group and significantly higher in the HBO group than in the normoxic group during repetitions 41–50 (P = 0.049), but not during the other repetitions (Figure 2).

Figure 2
Figure 2:
Changes of voluntary plantar flexion torque during the FTs before and after interventions. Data (average of 1 second during contraction) were pooled for consecutive set of 10 contractions over subjects. Significant difference between HBO and normoxic group was observed only contractions 41–50 (*p ≤ 0.05). Values (mean ± SE) were expressed as percent of initial value (average of 4–10 contractions). FT = fatigue test; HBO = hyperbaric oxygen.

Electromyography During the Fatigue Test

Root mean square values tended to decrease as the number of repetitions increased in both groups (Figure 3). For the soleus, RMS values during repetitions 41–50 in the FT before intervention decreased to 81.4 ± 9.9% and 70.6 ± 6.4% of the initial values during repetitions 4–10 in the HBO group and normoxic group, respectively. Root mean square values during repetitions 41–50 in the FT after intervention decreased to 85.9 ± 4.1% and 75.2 ± 5.2% of the corresponding initial values in the HBO group and normoxic group, respectively. Differences between the groups were significant only during repetitions 31–40 (P = 0.034). For the MG, RMS values during repetitions 41–50 in the FT before intervention decreased to 63.6 ± 6.3% and 55.1 ± 5.8% of the initial values during repetitions 4–10 in the HBO group and normoxic group, respectively. Root mean square values during repetitions 41–50 in the FT after intervention decreased to 75.9 ± 4.7% and 62.5 ± 4.5% and differences between the groups were significant only during repetitions 41–50 (P = 0.049). For the LG, RMS values during repetitions 41–50 in the FT before intervention decreased to 68.2 ± 5.8% and 56.7 ± 6.2% of the initial values during repetitions 4–10 in the HBO group and normoxic group, respectively. Root mean square values during repetitions 41–50 in the FT after intervention decreased to 74.8 ± 6.3% and 67.7 ± 8.7%, but the differences between the groups were not significant throughout the test. Although the RMS values in the soleus, MG, and LG in the HBO group changed less compared with the normoxic group, the plantar flexion torque during repetitions 41–50 corresponded with the RMS value during repetitions 41–50 in the MG alone in the FT after intervention. Therefore, the RMS value in MG corresponded most with the plantar flexion torque.

Figure 3
Figure 3:
Changes in RMS values of soleus, MG, and LG muscles during the FTs before and after interventions. Data (average of 1 second during contraction) were pooled for consecutive set of 10 contractions over subjects. Significant differences between HBO and normoxic group were observed with contractions 31–40 in soleus muscle and with contractions 41–50 in MG muscle after intervention (*p ≤ 0.05). Values (mean ± SE) were expressed as percent of initial value (average of 4–10 contractions). RMS = root mean square; MG = medial gastrocnemii; LG = lateral gastrocnemii; FT = fatigue test; HBO = hyperbaric oxygen.

The MPF values in the soleus during repetitions 21–30, 31–40, and 41–50 were similar in both groups. Mean power frequency values in the MG and LG during repetitions 11–20 were also similar in both groups, whereas those during repetitions 31–40 and 41–50 were higher in the HBO group than in the normoxic group, albeit not significantly (Figure 4). There were also no significant differences between the MPF values in the soleus, MG, and LG during FT before and after intervention.

Figure 4
Figure 4:
Changes of MPF values of soleus, MG, and LG muscles during the FTs before and after interventions. Data (average of 1 second during contraction) were pooled for consecutive set of 10 contractions over subjects. There were no significant differences between the groups. Values (mean ± SE) were expressed as percent of initial value (average of 4–10 contractions). MPF = mean power frequency; MG = medial gastrocnemii; LG = lateral gastrocnemii; FT = fatigue test.

Twitch Interpolation Test

Tables 1 and 2 show the values of test 1, test 2, and test 2/test 1 ratio (before intervention) and those of test 3, test 4, and test 4/test 3 ratio (after intervention), respectively, in both groups. Plantar flexion torque during MVC of the triceps surae muscles, activation, and the control twitch torque, contraction time, and half relaxation time values of the twitches induced by electrical stimulation at rest are shown with the corresponding RMS and MPF values of the EMG signals in the soleus, MG, and LG during MVC in Table 1. Both test 2/test 1 ratio (before intervention) and test 4/test 3 ratio (after intervention) results revealed decreased MVC, activation, and control twitch torque and increased contraction time and half relaxation time values in both groups. No significant differences between the groups in both test 2/test 1 ratio and test 4/test 3 ratio were observed in any of the variables shown in Table 1.

Table 1
Table 1:
Selected variables of MVC and twitch interpolation test.*†
Table 2
Table 2:
Amplitude and duration of M wave evoked by twitch interpolation.*†

The amplitude and duration of the M waves evoked by electrical stimulation of the triceps surae muscles at rest are shown in Table 2. M wave amplitude decreased in both groups before and after intervention. However, no significant differences between the groups in both test 2/test 1 ratio and test 4/test 3 ratio were observed in any of the variables shown in Table 2.

Discussion

The main finding of this study is that the decreases in the plantar flexion torque during repetitions 41–50 in the FT after intervention were significantly smaller in the HBO group compared with the normoxic group. Furthermore, the RMS values of the EMG signals of the soleus during repetitions 31–40 and MG during repetitions 41–50 in the FT after intervention were significantly smaller in the HBO group compared with the normoxic group. However, the plantar flexion torque and EMG during MVC and the plantar flexion torque, EMG, and M wave in response to electrical stimuli before and after intervention were not significantly different between the groups. These results suggest that HBO treatment contributes to sustained force production due to suppress the muscle fatigue progression, rather than to short-term maximal force production. Consequently, this study shows for the first time the effect of HBO treatment on endurance for isometric contractions with the plantar flexors.

Electromyographic signal has usually been explained by changed recruitment, synchronization of motor unit, and variations of the motor unit discharge (7,12,16,20). Decreases in motor unit recruitment, synchronization, and firing rates are thought to be the main reasons for the decreased RMS values of the EMG signals in active muscle groups during muscle fatigue-causing maximal contraction exercise (10). Changes in RMS values and frequencies of EMG during incremental exercise under hyperoxic conditions in humans suggest that hyperoxia increases motor unit synchronization and firing rates (15). Although no similar studies in HBO have been reported, the elevated muscle oxygen levels at the beginning of the FT after intervention in this study likely increased the synchronized firing and firing rates of motor units in active muscle groups, particularly in the MG in the HBO group, and this may have contributed to the reduced levels of fatigue during the exercise in the soleus and MG in the HBO group compared with the normoxic group.

No significant differences were observed in control twitch torque, contraction time, or half relaxation time values between the groups after the FT after intervention (test 4), suggesting that HBO treatment did not alter the contractile properties of the muscles. Furthermore, the differences in the M waves and MPF of EMG in the soleus, MG, and LG were not significant between the groups. The effect of HBO treatment on the muscle contractile properties was negligible after fatiguing contractions.

Exercise-induced muscle injury occurs immediately after exercise with strong eccentric contractions (9). Magnetic resonance imaging analysis showed short-lasting increases in T2 immediately after exercise, although fatiguing concentric exercise was performed, suggesting edema in the exercise-damaged muscle (24). Hyperbaric oxygen could reduce edema in the quadriceps muscle of the exercised leg after high-intensity eccentric exercise. This study also set the protocol of maximal intermittent plantar flexion exercise. Immediate HBO treatment could reduce exercise-induced edema, resulting in a smaller decrease in muscle force in the HBO group compared with the normoxic group.

Hypoxia reduces handgrip MVC force (23) and was suggested to attenuate activation in regions associated with vasomotor areas of the brain (8). In addition, reduced oxygen delivery to the locomotor and respiratory muscles enhances inhibitory feedback on central command (1). Amann and Dempsey (2) have proposed that the magnitude of the inhibitory neural feedback is highly sensitive to muscle oxygen delivery. Moreover, hyperoxia activates group IV muscle afferents (4,19).

Thus, it is possible that in this study, the fatigue-inducing effect through activation of group IV muscle afferents occurred with the delayed effect on muscle fatigue progression attributed to the decreased inhibitory afferent feedback on central command in the HBO group. The delayed effect on muscle fatigue progression possibly exceeded the fatigue-inducing effect in the HBO group, resulting in smaller reductions in plantar flexion torque compared with the normoxic group. However, we could not find significant differences in muscle activation after the FT after intervention (test 4) between the groups (Table 1). Whether or not the above events were attributed to central nervous system activity remains unknown. Nevertheless, it is likely that the reduction in the central command during the FT after intervention was smaller in the HBO group than in the normoxic group, resulting in a smaller decrease in muscle force in the former group than in the latter group.

In conclusion, the results of this study suggest that HBO treatment contributes to the endurance of muscle force in maximal isometric contractions with repetitive movement (50 repetitions). The results also suggest that HBO treatment after muscle fatigue is beneficial for sustained force production, rather than for short-term maximal force production. Although this is the first study to provide data that suggests a positive effect of HBO treatment on endurance in repetitive muscle contractions, the effects of HBO on the recovery from muscle fatigue are unclear. Considering the limited findings in this study, more in-depth investigation of the benefits of HBO treatment for conditioning athletes is warranted.

Practical Applications

According to the results of this study, we suggest that application of HBO to reduce muscle fatigue, for example, due to a locally applied heavy load to the triceps surae muscles. An athlete with excess fatigue of the agonist muscles could consider HBO as a treatment option to reduce muscle soreness and prevent muscle damage during training or competition. Hyperbaric oxygen could be useful, in particular, in sports involving repeated jumping, such as volleyball or handball, which will lead to increased fatigue of the lower leg muscles. The circumstances of HBO application during training or competition should be arranged for actual practical application for athletes.

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Keywords:

repetitive exercise; voluntary contraction; twitch interpolation; plantar flexion torque; surface electromyography; single-blind design

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