Acute bouts of high-force eccentric muscle actions can cause delayed onset muscle soreness (DOMS) (1,2,6,7,12,15,16,22,25), which apart from muscle pain, is signified by morphological changes and elevations of muscle proteins, reflecting muscle damage, muscle stiffness, decrements in force production, and edema formation (2–4,6,7,13,14,19).
The precise mechanisms underlying the development of DOMS remain unresolved, though a multitude of factors have been suggested as possible causes in the development of DOMS (2,4,7,12). Concomitant with the several proposed theories regarding the development of DOMS (5,8,27) are numerous suggestions for the treatment of DOMS, including anti-inflammatory drugs, massage, and light exercise (10,11,23,28,29,33).
The use of hyperbaric oxygen therapy (HBOT) to treat exercise-related injuries has recently become popular among elite athletes and professional sports teams (20, 30). HBOT is a clinical treatment in which patients breathe 100% oxygen at elevated ambient pressures, ensuring that the tissue partial pressure of oxygen is substantially elevated (18). The ability of HBOT to provide hyperoxygenated blood to damaged ischemic tissue has been shown to accelerate healing (9).
In view of anecdotal reports of accelerated recovery rates from various sports injuries including DOMS (20), we performed a controlled blinded study to investigate the potential benefits of HBOT on the rate of recovery of muscle strength, the duration of the perceived muscle soreness, and edema.
Twenty-four healthy male volunteers (age 20–35 yr) participated in the study. The subjects were informed that the protocol of this experiment would involve strenuous exercise, which would induce muscle soreness in their biceps brachii and brachialis muscles. Volunteers who had prior knowledge of exercise induced muscle soreness but who stated that they had not performed eccentric training of the elbow flexors in the past 3 months were allowed to participate. The protocol was approved by the University of Ljubljana Ethics Review Committee. Subjects provided their informed consent to participate in the study.
The study was conducted using a randomized, blinded procedure. The subjects were randomly assigned to either the hyperbaric oxygen group (HBOT) or placebo group.
All subjects were initially (preexercise) tested for maximal isometric strength (maximal voluntary contraction, MVC) of the elbow flexors of their right arm. Each subject then completed one high-force eccentric workout of the elbow flexor muscle group of their right arm. Ten minutes after the maximal workout and then daily during 6 successive days, subjects’ MVC was retested. Subjects also reported to the laboratory on the 8th and 10th days after the maximal workout. Subjects were exposed to a hyperbaric environment for 60 min after the postexercise strength test and before the retests on the first 6 days after the eccentric workout. At an ambient pressure of 2.5 ATA, subjects in the placebo group inspired a normoxic gas mixture containing 8% oxygen (PIO2 = 0.2 ATA). At the same ambient pressure of 2.5 ATA, subjects in the HBOT group inspired 100% oxygen (PIO2 = 2.5 ATA) for 60 min. On each testing day, arm circumference was measured and each subject was also asked to rate the muscle soreness.
By definition, hyperbaric oxygen therapy (HBOT) implies the administration of 100% oxygen intermittently at pressures greater or equal to 1.4 ATA for periods equal to or greater than 60 min (31). Clinically, hyperbaric oxygen therapy is limited to a maximal partial pressure (PO2) of 3.0 ATA (17). Although there are general guidelines prescribing the dosage of oxygen for specific indications (31,32), HBOT may be tailored for individual patients depending on their response to the hyperbaric oxygen therapy. For a given indication, an optimal HBOT protocol must be determined in terms of absolute pressure, duration of exposure, frequency of treatments, and total number of treatments. Exceeding the optimal HBOT protocol provides no advantages, due to the increased toxic effects of oxygen. In view of the risks associated with HBOT and no current guidelines regarding the use of hyperbaric oxygen therapy for DOMS, a conservative protocol was chosen for the present study (pure oxygen breathing at a pressure of 2.5 ATA for 60 min). We reasoned that for the treatment to be of any practical benefit to athletes, it should provide an indication of enhanced recovery from exercise-induced DOMS within several days of the exercise. Consequently, HBOT was administered once a day for 7 d.
For each subject, during one of their treatments, a transcutaneous PO2 (TcPO2) electrode attached to the skin over the biceps brachii muscle provided an indication of the magnitude of tissue oxygenation during the treatment.
All subjects were naive regarding their group designation. Also, one of the four investigators, who conducted the final statistical analyses, was not involved in the actual treatments and kept naive with regard to the treatments received by the subjects while performing the analysis.
Test of MVC.
Subjects were seated into a modified “preacher curl bench” (Barotech d.n.o., Ljubljana) similar to that described by Clarkson et al. (6), to test for preexercise MVC. The height of the seat was adjusted so that the subject’s back was vertical, and both arms were over the armrest such that the top edge of the armrest fit snugly into the subject’s armpits inhibiting twisting of the torso. With the left hand, the subject grasped the bottom edge of the armrest and with the right hand, palm up, grasped the handle connected to the force transducer on the lever arm. To maintain each subject’s elbow at an angle of 90° throughout the strength test, chains connecting the bench and lever arm were adjusted until the proper angle was achieved using a goniometer. Once a proper chain length was determined, it was then used for that subject for each MVC maneuver throughout the study.
The subject was asked to isometrically contract the elbow flexors with maximal effort for 5 s. The force produced was measured by a force transducer (Nobel Elektronik Force Transducer Type KRG-4, Karskoga, Sweden). The signal was amplified and displayed continuously.
Each subject performed three separate trials with a 5-min rest period between trials. During each trial, the subject was instructed to maintain a constant body position and use only the right elbow flexor muscles to perform the strength test. During each strength test, all subjects were verbally encouraged to perform a maximal effort.
Ten minutes after the high-force eccentric workout and then once daily for 10 d, the subjects were retested for MVC, using the same protocol.
Maximal eccentric workout.
After the initial measurement of maximal isometric strength, the subjects performed a high-force eccentric workout of the right elbow flexors. The subjects were again seated in the modified preacher curl bench in the same manner as for the isometric strength test. However, during the high-force eccentric exercise bout, the chains that maintained the constant lever arm position and elbow angle were disconnected. Each repetition of the high-force eccentric workout commenced with the subject’s elbow fully flexed and the experimenter holding the end of the lever arm. The experimenter slowly pulled down on the end of the lever as the subject contracted the elbow flexor muscles. This slowly and steadily forced the subject’s arm into extension to approximately 150°. During this procedure, the subject was instructed to resist the movement with maximum effort by continually contracting their elbow flexors. Each repetition took approximately 3–4 s to complete the full range of motion. With the mechanical advantage afforded by the lever system, the investigator was able to provide proper resistance to maintain a relatively constant rate of movement throughout the entire range of motion. At the end of the range of motion, the subject calmly and against no resistance returned their arm to the starting fully flexed position while the experimenter raised the lever arm to its starting position. Subjects performed 6 sets of 12 maximal effort repetitions. Rest periods of 3 s between repetitions and 5 min between sets were provided.
Placebo treatment group.
Immediately after the postexercise MVC test and for the following 6 d, subjects were exposed to a hyperbaric environment (a total of 7 hyperbaric exposures). For each exposure, the subjects were seated inside a Marine Dynamics (Long Beach, CA) multiplace hyperbaric chamber. The chamber was then compressed with air to a pressure of 2.5 ATA at a rate of approximately 0.3–0.5 ATA·min−1. During compression, the subjects breathed the ambient air in the chamber. Once at a pressure of 2.5 ATA, the subjects were fitted with an aviator style gas mask, which formed a tight seal around the mouth and nose, and inspired a gas mixture containing 8% O2/92% N2, which was normoxic at 2.5 ATA (PIO2 = 0.2 ATA). The gas was delivered through a series of regulators to the masks from high-pressure cylinders external to the chamber. Subjects remained at 2.5 ATA breathing this gas up to the 60-min mark from the time compression began. With a normal 3–5 min time for compression, this resulted in each treatment lasting for 55–57 min. At the 60-min mark, the subjects removed their masks and again began breathing the ambient air of the chamber and decompression was initiated. Decompression was conducted according to the Defence and Civil Institute of Environmental Medicine (DCIEM) Dive Decompression Tables for an equivalent air depth (EAD) of 20 meters of sea water; thus accounting for the elevated PIN2 in the control condition. The decompression required a 2-min stop at 6 m and an 11-min stop at 3 m.
The compression and decompression procedures for the HBOT group was identical with the procedures for the placebo group, thus making it impossible for the subjects to determine their group designations. In contrast with the placebo group, subjects in the HBOT group inspired 100% oxygen, which was delivered to the masks from high-pressure cylinders external to the chamber.
Perceived muscle soreness.
Subjects were requested to give a subjective rating of the muscle soreness in their right elbow flexors. The testing occurred before the preexercise isometric strength test and immediately after each hyperbaric exposure on days 1–7 and at anytime on days 8–10. They were instructed to attempt to fully extend their arm at the elbow and then rate the soreness they experienced while performing this extension. The ratings were based on a visual analog scale (VAS scale). The subjects were presented with a form containing a 10-cm line. The limits of the line were identified as “no pain at all” and worst pain I could possibly feel.” The subjects were instructed to mark the location on the line, relative to these limits, which reflected their perception of muscle soreness.
Arm circumference measurement.
The measurements of arm circumference were taken before each MVC test using a standard metric tape measure, around the right upper arm at the midpoint of the distance from the lateral epicondyle of the humerus to the acromion. A mean of three measurements was obtained during every testing period. During the measurements the arm was extended.
During one hyperbaric treatment between days 2 and 5 of the experiment, the transcutaneous oxygen content in each subject’s upper right arm was measured with a transcutaneous PO2 monitoring system (TINA Radiometer Transcutaneous Monitor TCM3, Copenhagen, Denmark). The electrode was fitted into a plastic ring attached to the skin above the biceps brachii muscle. The ring was filled with electrolyte solution and the membraned sensor head fitted into the ring. The monitor gave continuous measurements while warming the skin under the sensor to a temperature of 44°C. Measurements were recorded until 15 min of relatively steady-state values were obtained.
Group differences regarding isometric strength, arm circumference and TcPO2 were analyzed using a two-way ANOVA. The VAS scores were compared using a nonparametric test (Mann-Whitney U-test).
There was a significant difference in TcPO2 measurements between groups (P < 0.001). The HBOT group recorded an average ± SD of 1420 ± 144 mm Hg, whereas the placebo group averaged only 91 ± 23 mm Hg (Fig. 1).
The eccentric workout reduced MVC similarly for both groups (P < 0.001), to approximately half their preexercise values (Fig. 2). The HBOT group attained an isometric strength drop from (mean ± SD) 25.1 ± 3.8 kp to 12.0 ± 4.6 kp, whereas the placebo group decreased from 24.6 ± 3.4 kp to 12.5 ± 3.7 kp.
The rate of recovery of MVC was similar and almost linear for the two groups over the 10 d period (Fig. 2). After 10 d, with 6 HBOT or placebo treatments on days 1 to 6, MVC recovered to 62% and 61% of preexercise MVC for the HBOT and placebo groups, respectively.
Perceived muscle soreness.
Muscle soreness described a bell-shaped curve (Fig. 3), attaining a peak 2-d after the eccentric workout in both groups (P < 0.001). There was no difference in the magnitude of soreness between groups overall or on any particular day during the testing period.
The peak swelling (i.e., increase in arm circumference, P < 0.001) occurred between days 3 and 5 with no difference evident between groups (Fig. 4).
The impetus for the present study was the increasing use of HBOT among athletes, to ameliorate exercise-induced DOMS and dysfunction. Our aim was to examine the influence of HBOT on muscle strength and perceived soreness after an exercise challenge by employing a protocol designed to eliminate potential experimenter bias and placebo effect. The findings of this study suggest that HBOT is of no benefit in the treatment of exercise-induced muscle dysfunction or DOMS.
An exercise regime incorporating repeated bouts of maximal eccentric muscle actions was chosen, because numerous studies have shown such a protocol to be effective in provoking marked DOMS (6,19,25), muscle injury, and compromised force (6,7,19,25,26). Although these events do not follow an identical time course, it is clear that both soreness and swelling, expressing an inflammatory response, increase over a few days subsequent to exercise. Our results confirm these previous findings and, furthermore, show that the responses are unaffected by HBOT. Hence, the magnitude of injury induced was similar in both groups, evident from the observations of no differences in preexercise isometric strength or in strength drop after the high-force eccentric workout. The observation that neither the rate, nor magnitude of recovery of isometric strength differed between groups indicates that HBOT did not accelerate the injury healing involved in strength restoration. This finding contrasts a single claim, reported in a non-peer-reviewed paper (J. R. Staples, Effect of intermittent hyperbaric oxygen on pain perception and eccentric strength in a human model injury. M.Sc. Thesis. University of British Columbia, Vancouver, Canada, 1996), supporting the efficacy of HBOT in ameliorating exercise-induced muscle dysfunction.
Similarly, perception of muscle soreness, peaking 2 d after the high-force eccentric workout showed no group difference, neither overall nor on any particular day. These results are in frank contrast to the various anecdotal reports of HBOT successfully alleviating muscle soreness in athletes (20).
The high-force eccentric exercise induced edema, as reflected in markedly increased arm circumference, exhibited a peak between days 3 and 5, with no difference between groups. This finding of an assumed increase in muscle water content accords with numerous previous reports demonstrating increases in muscle cross-sectional area using magnetic resonance imaging (24).
Edema is a result of either an increase in vascular permeability of small blood vessels, or a leakage of intracellular fluid into the extracellular space (26), resulting in tissue hypoxia, due to the increased oxygen diffusion distance from the capillaries to some cells, and the increased interstitial pressure around the capillaries due to the fluid accumulation (21). The ensuing ischemia limits energy production due to the lack of oxygen for ATP production (21), which concomitant with the increased energy demands of injured tissue, leads to impaired healing rates (9). With HBOT, the oxygen diffusion distance from the capillaries can be up to four times greater than normal due to the larger pressure gradient between capillary and tissue PO2, which increases the number of cells that can be oxygenated when cellular oxygenation is limited by edema (9). It could be hypothesized that, by ensuring adequate cellular oxygenation, cellular energy production would be maintained, allowing the cell to fuel its ATP driven pumps and channels, thus enhancing the reabsorption of fluid from the extracellular space, and decreasing the edema (18). In addition, the secondary vasoconstrictory effect of hyperoxygenated blood, capable of reducing blood inflow by 20% without decreasing oxygen delivery, was also considered capable of reducing edema, by decreasing the intravascular hydrostatic pressure, and establishing a more favorable pressure gradient for fluid movement out of the interstitial space back into the capillaries. Also, oxygen dissolved in plasma is not limited by the flow of red blood cells and can thus travel through smaller spaces, such as damaged or blocked capillaries often found in damaged tissues, reaching areas which are inaccessible to hemoglobin bound oxygen (21).
In contrast to studies that have demonstrated an HBOT-induced reduction of edema formation in burns and postischemic tissues (18), HBOT was not effective in minimizing the edema formation associated with exercise-induced muscle injury. Possibly the edema induced was not of sufficient magnitude to establish the increased diffusion distances and increased interstitial pressure, which might promote tissue hypoxia (21).
It could also be hypothesised that HBOT might improve recovery from exercise-induced muscle damage by accelerating connective tissue repair, which in turn may potentially serve to relieve pain (16). A wounded tissue may have many small ischemic areas due to microvascular damage and edema formation, even if the overall oxygen tension of the tissue appears normal (9). Thus, during DOMS, the synthesis of new collagen to replace the damaged collagen may be delayed. In ischemic tissue, HBOT provides oxygen to relieve the hypoxia (9). Because the problem with the posttranslational processing of collagen is reversible with an elevation of the oxygen tension, it follows that elevating the oxygen tension of the damaged area should increase the rate of recovery by promoting collagen production and angiogenesis (21). Despite the substantially elevated tissue oxygen tension, confirmed with TcPO2 measurements, HBOT did not induce any sign of accelerated healing rate.
It is noteworthy that alternative treatments, including antiinflammatory drugs, massage, and light exercise have failed to demonstrate a consistent therapeutic effectiveness in reducing muscle soreness and the associated inflammatory processes (10,11,23,28,29,33), confirming the notion that the mechanisms explaining the functional impairment associated with DOMS are not known in detail. Our approach was descriptive, rather than mechanistic, and aimed at addressing the issue of whether HBOT, by increasing tissue oxygen pressure, would reduce exercise-induced DOMS and hence improve recovery. Results showed this was not the case.
It is unlikely that the finding of no effect of HBOT on recovery from DOMS may be attributed to the unsuitability of the chosen HBOT protocol (60 min at 2.5 ATA, once a day for 7 d). HBOT protocols for all indications currently approved for treatment with hyperbaric oxygen vary in terms of the pressure and duration of exposure to hyperbaric oxygen, and the frequency and total number of treatments. The differences in the nature of the protocols do not imply that for a given indication only one protocol will provide improvement but that the recommended protocol has been found to provide the optimal improvement. Exceeding the optimal oxygen dose for a given indication will not yield any further benefits but only increases the toxic effects of oxygen (17). In the event that HBOT revealed enhanced recovery from DOMS, further studies would have been necessary to elucidate whether the chosen protocol provided an optimal dosage of oxygen for DOMS or whether the optimal dosage was exceeded.
Recovery of muscle strength after exercise-induced injury may require several weeks. Indeed, Howell et al. (19) reported that the half-time of recovery in their subjects, who experienced a 35% exercise-induced muscle strength loss, was 5–6 wk. Our findings regarding the recovery of muscle strength in our subjects 10 d after the exercise-induced injury are in agreement with the observations of Howell et al. (19). In view of the findings that complete recovery of muscle strength may require many weeks, it could be argued that administering HBOT over a 7-d period is insufficient to render any benefits. However, from a practical perspective, HBOT administered to an athlete to enhance recovery of muscle strength from exercise-induced injury should provide an indication of significant improvement in the rate of recovery within several days. The associated toxic effects of hyperbaric oxygen would not warrant continued treatment, especially in view of our present findings of no effect of HBOT within 10 d after the exercise-induced injury.
In conclusion, the results of the present study demonstrate that hyperbaric oxygen therapy does not enhance recovery of exercise-induced loss of muscle strength nor the recovery from delayed onset muscle soreness. In view of our findings and the known risks associated with inspiring pure oxygen at elevated ambient pressures, the use of HBOT among elite athletes to minimize the effects of DOMS is not warranted and should be discouraged.
The authors are indebted to Mr. Matija Jager and Barotech d.n.o. for technical support.
This study was supported, in part, by the Ministry of Science and Technology of Slovenia and by Biomed d.o.o. (Ljubljana, Slovenia).
Present address for J. A. Exner: Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada.
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