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Medicine & Science in Sports & Exercise:
Basic Sciences: Original Investigations

Effect of resistance exercise on free radical production

McBRIDE, JEFFREY M.; KRAEMER, WILLIAM J.; TRIPLETT-McBRIDE, TRAVIS; SEBASTIANELLI, WAYNE

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Laboratory for Sports Medicine/Department of Kinesiology, Noll Physiological Research Center, Center for Sports Medicine, Center for Cell Research, The Pennsylvania State University, University Park, PA 16802

Submitted for publication February 1997.

Accepted for publication August 1997.

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Abstract

The purposes of this investigation were to see whether free radical production changed with high intensity resistance exercise and, secondly, to see whether vitamin E supplementation would have any effect on free radical formation or variables associated with muscle membrane disruption. Twelve recreationally weight-trained males were divided into two groups. The supplement group (S) received 1200 IUs of vitamin E once a day (3 × 400 IU·d-1) for a period of 2 wk. The placebo group (P) received cellulose-based placebo pills once a day for the same period of time. Creatine kinase activity was significantly elevated between preexercise and immediately postexercise, 6 h postexercise, and 24 h postexercise for both groups. The placebo group also had a significant increase in creatine kinase activity at 48 h postexercise. There was a significant difference in creatine kinase activity between the groups at 24 h after exercise. Plasma malondialdehyde significantly increased from preexercise levels for the P group at 6 and 24 h postexercise. Plasma malondialdehyde concentrations significantly increased in the S group between preexercise and immediately postexercise levels. This study indicates that high intensity resistance exercise increases free radical production and that vitamin E supplementation may decrease muscle membrane disruption.

Oxygen is essential for human life but in some forms can be damaging to the body (10,15,32). The cell damage free radicals can cause is of interest because of its suggested relationship to certain disease states such as cancer and cardiovascular disease(7,13,19,27,34). Investigations in these areas have begun to focus on possible free radical formation during exercise and its relation to exercise-induced muscle damage(6,9,30). Significant increases in free radical production during exercise can be indirectly measured by the presence of lipid peroxidation products, primarily malondialdehyde (MDA)(3,9,30). Several studies have tried to determine, through the measure of lipid peroxidation products, whether free radical formation does increase; they have met with varying results(20,26,36,40). Some studies have looked at repetitive static muscle actions and also concentric and eccentric muscle actions (35,37). These studies reported no difference in markers for free radical production. However, these studies used resistance exercise protocols that would be considered very low intensity and also involved a limited number of muscle groups. To date, no known studies have measured changes in lipid peroxidation parameters in response to a high intensity resistance exercise protocol involving several of the body's major muscle groups.

Plasma MDA measurements during exercise have also been correlated with creatine kinase, a marker for muscle damage (20). There has been an attempt to establish a relationship between free radicals and muscle damage. Studies have shown that increased lipid peroxidation occurs in patients with muscular dystrophy (10,19). These studies indicate that free radical formation may play a role in exercise-induced muscle damage.

Certain vitamins within the body have been suggested to play vital roles as antioxidants. Vitamin E, which is a term used to describe a specific group of tocotrienols and tocopherols, has been described as being unique in its mechanism of action in comparison with all other vitamins as a cellular membrane bound antioxidant (2). Studies have looked at the effect of antioxidant supplementation on reducing lipid peroxidation associated with exercise and reported a significant effect(21,40). Athletes supplemented with vitamin E and C showed a 25% reduction in tissue damage as marked by decreased levels of cytoplasmic enzymes, creatine kinase, and lactate dehydrogenase(14). These studies are speculative but seem to indicate that free radical damage to cellular membranes that occurs as a result of exercise may be decreased by the use of these vitamins.

Therefore, the primary purpose of this study was to determine whether lipoperoxide plasma measurements ([TBA]2-MDA adduct), as a marker for free radical production, would change during or after an intense resistance exercise bout. The secondary purpose of the study was to determine whether antioxidant vitamin supplementation (vitamin E) before the exercise bout would have any significant effect or relationship to changes in lipoperoxide plasma measurements or variables associated with muscle damage (i.e., creatine kinase, perceived soreness ratings).

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METHODS

Subjects. Men between the ages of 18 and 30 yr of age were asked to volunteer for this investigation. All subjects were required to be recreationally weight trained with resistance training experience of at least 1 yr. Prior approval by the Institutional Review Board (IRB) for the Use of Human Subjects at the Pennsylvania State University was obtained. Each subject had the risks of the experiment explained to them and signed an informed consent document. This study conformed with the policy statement regarding the use of human subjects as published by Medicine & Science in Sports& Exercise. Subjects were medically screened and none had any medical problems (e.g., orthopaedic, endocrine, cardiovascular) that would confound the results of this investigation. The subject characteristic variables were as follows for each of the experimental groups (mean ± SE): 1) Placebo Group: age 22.0 ± 0.85 yr; height 177.17 ± 1.39 cm; body mass 81.22 ± 4.70 kg; body fat 10.58 ± 1.54%; 2)Supplement Group: age 21.17 ± 0.65 yr; height 178.45 ± 2.31 cm; body mass 78.51± 4.13 kg; body fat 11.60 ± 1.59%. No significant differences were observed between groups for any of these variables. Subjects were matched for training exposure, strength, and body size.

Experimental design. Twelve men were matched and randomly placed into one of two treatment groups of six subjects each. One group received a vitamin E supplement for a period of 2 wk before the test date [S]. The other group received a placebo (i.e., identical looking cellulose capsule) for the same period of time (P). This supplementation regimen consisted of 992 mg·d-1 of vitamin E in the form of RRR-d-alpha-tocopherol succinate (1200 IU, 800 TE) (Twin Laboratories, Inc., Ronkonkoma, NY). Individual 3-d diet diaries were used and analyzed to ensure no significant differences in dietary vitamin E intake existed before the supplementation period. Initially, a dietary history questionnaire for the previous 6 months was given to subjects to identify any possible abnormal intakes in vitamin E during that period. A diet diary was also obtained for 3 d during the 2-wk supplementation period to quantify average vitamin E intake for both treatment groups. Each subject was instructed and provided with specific verbal instructions and procedures for recording dietary intake. This instruction included how to record portion size using household measure, combination foods, preparation technique, and nutrient content descriptions (i.e., light, fat free, lean, reduced, etc.). A Nutritionist IV computer program was used for all dietary analysis (N-squared Computing, First Databank Division, The Hearst Corporation, San Bruno, CA). This software contains a current data base of over 13,000 foods including products from national fast food chains.

The test consisted of a heavy resistance exercise protocol that was similar to a previously described 10/1 protocol used by Kraemer et al.(23). Total work was matched for both groups according to a previously described method (23). A one-repetition maximum (RM) test and a 10RM test was administered for each exercise. Subjects were completely familiarized with the exercise protocols before the start of data collection and supplementation. The exercise habits of the subjects were maintained throughout the testing and supplementation period. Subjects were not allowed to train for 48 h before or after the acute exercise bout. Blood samples were obtained 5 min before exercise (pre-exercise), halfway through the exercise protocol (mid-exercise), immediately postexercise, and at 6, 24, and 48 h postexercise. Perceived soreness ratings were obtained using a scale of 0 (no soreness) to 10 (extremely sore). This scale was similar to that used in previous studies of muscle soreness (5,6). Perceived soreness ratings were obtained from each subject at 6, 24, and 48 h after exercise. The bench press, shoulder press, calf raises, and leg press exercises were performed on a Universal Gym (Universal Gym Equipment, Cedar Falls, IA). The bent-over rows and arm curls were performed as free weight exercises with a standard bar and weights. The Tru-Squat (Southern Exercise Equipment, Shelbyville, TN) exercise was performed on a special machine that simulates the squat exercise. The resistance exercise protocol consisted of eight exercises performed in a circuit fashion. This means that one set was performed on each exercise then the cycle was repeated. A circuit of warm-up sets consisting of eight to ten repetitions was performed before the three-set circuit workout using 50% of the individual's previously determined 1RM. This experimental heavy resistance exercise protocol was performed using each individual's predetermined 10 RM for each exercise on the first set. The weight lifted was then adjusted based on the familiarization workout to account for muscle fatigue. This was necessary to maintain the performance of ten repetitions for every set. A total of three sets was performed for each exercise with a 2-min rest between each set on the first circuit of eight exercises. For the second circuit a 1.5-min rest period between sets was used, and a 1-min rest period was employed on the third circuit of eight exercises.

Blood was obtained from an antecubital vein by the Vacutainer (Baxter, Obetz, OH) System using a 20 gauge needle. The blood was then distributed into the appropriate tubes for the various biochemical analyses. Blood was removed from an EDTA tube (Baxter, Obetz, OH) for immediate analysis of hematocrit and lactate. Whole blood was removed and immediately stored in Eppendorf(Sarstedt, Newton, NC) tubes at -85°C for analysis of hemoglobin. Blood used for analysis of creatine kinase activity (CK), and lipoperoxides([TBA]2-MDA adduct) was transferred to a sealed glass tube, allowed to clot at room temperature, and centrifuged at 1500g for 15 min at 4°C. The plasma was then separated and stored in Eppendorf tubes at-85°C to be later analyzed. Samples were thawed only once for analysis.

Hematocrit was analyzed using a standard microcapillary (Baxter, Obetz, OH) technique. All samples were run in duplicate. If the variance between samples was greater than 1% a third measurement was obtained. Hemoglobin concentrations were determined in duplicate by a spectrophotometric method(Sigma Chemical Co., St. Louis, MO). Intra- and Inter-assay variance was less than 5% for the hemoglobin analysis. Plasma volume shifts were determined using hematocrit and hemoglobin values by a method described by Dill and Costill (8). Average plasma volume shifts for all time points measured were less than 10% with no difference between groups. Lactate was measured using a YSI 1500 L-lactate analyzer (Yellow Springs Instruments, Yellow Springs, OH). Samples were run in duplicate. Intra-assay variance was less than 5%.

For determination of plasma lipoperoxides ([TBA]2-MDA adduct) a variation of a method by Wong et al. was used (45). A phosphoric acid solution (0.44 mol·L-1, Sigma Chemical) and a thiobarbituric acid solution (42 mol·L-1, Sigma Chemical) were added to the plasma samples. The samples, controls, and standards were placed in a water bath (100°C) for 60 min and then placed in an ice water bath(0°C) until analysis. A methanol-NaOH (Sigma Chemical) solution was added to the boiled samples. The samples were then centrifuged (5000 rpm, 5 min) to precipitate the plasma proteins. The protein-free plasma was extracted and the absorbance was read at 532 nm using a Gilfor Stat Star spectrophotometer(Sigma Chemical). Blanks and 1,1,3,3-tetraethyoxypropane (TEP, Sigma Chemical) standard samples were used to prepare a calibration curve. All samples were run in duplicate. Intra-assay variance was less than 5% for MDA analysis.

Total plasma creatine kinase activity (CK) was determined in duplicate by using a colorimetric assay method and a Gilfor Stat Star spectrophotometer. All samples were run in duplicate. Inter- and intra-assay variance was less than 5% for CK analysis.

Statistical analyses of within-group data was achieved through the use of a repeated measures ANOVA. Statistical analyses of between-group data was achieved through the use of a factorial ANOVA. A Fisher PLSDpost-hoc test was used in all pairwise comparisons. An adequate statistical power for the study of 0.59 was observed for the N size used in this study. A correlational matrix was used to determine if there were any significant relationships between selected variables. Statistical significance was P ≤ 0.05.

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RESULTS

There were no significant differences in average weight lifted for each set for each exercise between the two treatment groups. The average percentage decrease in the mean weight lifted for both groups between set 1 and set 2 for all exercises was 7.72%. The average percentage decrease from set 1 to set 3 for all the exercises was 20.00%. The average percentage of the 1RM for all the exercises for both groups for set 1 was 75.27%, for set 2 it was 69.97%, and for set 3 it was 62.15%. There was no significant difference in average total work in J (J) completed per subject (P = 60,863.03 ± 8800.05 J; S = 57,355.09 ± 8487.49 J) between groups.

Whole blood lactate concentrations significantly increased at mid-(P = 16.253 ± 0.826 mmol·L-1, S = 13.523± 1.379 mmol·L-1) and immediate postexercise (P= 18.588 ± 0.954 mmol·L-1, S = 16.001 ± 1.233 mmol·L-1) time points for both groups from preexercise levels(P = 1.713 ± 0.411 mmol·L-1, S = 1.448 ± 0.247 mmol·L-1). There were no significant differences in whole blood lactate concentrations between groups for any of the time points measured. The rating of perceived exertion (RPE) obtained was not significantly different between groups at the mid- (P = 7.083± 0.961; S = 7.75 ± 0.544) or immediately postexercise(P = 8.5 ± 0.671; S = 8.5 ± 0.563) time points.

Creatine kinase activity was significantly higher at immediately post-, 6 h post-, 24 h post-, and 48 h postexercise for the placebo group. Creatine kinase activity was significantly higher at immediately post-, 6 h post-, and 24 h postexercise for the supplement group. There was a significant difference in the creatine kinase activity between the two groups at 24 h postexercise. These data are shown in Figure 1. The supplement group had significantly lower creatine kinase activity in comparison with the placebo group. Perceived soreness ratings obtained at 24 h postexercise(P = 3.25 ± 0.883; S = 2.333 ± 0.803) and 48 h postexercise (P = 2.75 ± 0.929; S = 2 ± 0.866) were not significantly different between the two groups.

Figure 1-Plasma crea...
Figure 1-Plasma crea...
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MDA was used as a quantitative marker for free radical interaction with cell membranes. There was a significant increase in plasma MDA concentration from pre-exercise levels at 6 h post- and 24 h postexercise for the placebo group (P). There was a significant increase in plasma MDA concentration from pre-exercise levels to immediately postexercise levels for the supplement group (S). There was no significant difference in the MDA concentration between groups for any of the measured time points. This is illustrated inFigure 2.

Figure 2-Plasma malo...
Figure 2-Plasma malo...
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There were no significant differences in the 3-d average vitamin E intake from food sources or caloric intake between groups before or during the supplementation period. The supplement group received an additional 1200 IUs of vitamin E during the supplementation period. The placebo group received an identical looking cellulose-based placebo pill that did not significantly affect the nutritional status of their diet during the supplementation period.

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DISCUSSION

The primary findings of this investigation were that free radical formation increases with intense heavy resistance exercise and that vitamin E is effective in attenuating accompanying muscle membrane disruption. This is the first study to examine the effects of a whole body heavy resistance exercise protocol on free radical formation and the effects of vitamin E supplementation.

The MDA response to the resistance exercise protocol in this study demonstrated a significant increase in free radical production. Vitamin E supplementation in this study resulted in a notable difference in the pattern and magnitude of the MDA measurements. These data indicate that vitamin E acted in a defensive manner, therefore decreasing the amount of free radical interaction with cellular membranes of the body. The creatine kinase changes observed in this investigation showed that muscle tissue disruption occurred well after the exercise bout. In addition, creatine kinase measurements in this investigation suggest that vitamin E supplementation resulted in a decreased amount of muscle membrane disruption following exercise.

The MDA response observed in this study is in agreement with some of the previous investigations involving aerobictype exercise(20,40). It is unclear at this time why both resistance exercise and aerobic-type exercise would result in similar increases in free radical production. It might be expected that the mechanisms for the increase in free radical formation during resistance exercise and aerobic-type exercise may be different. Only two open investigations in the current literature have examined resistance-type exercise and free radical formation. Both studies reported no increase in free radical formation(35,37). This may be a result of lighter loads and a smaller amount of muscle tissue activation. The lack of any significant physiological stress associated with the previous investigations was marked by the lower lactate levels, the lower volume of exercise, and the lower amount of muscle activation that characterized the exercise protocols used. Apparently the intensity of the exercise protocol is vital to cause measurable changes in plasma MDA.

The effectiveness of vitamin E is in agreement with previous investigations involving antioxidant supplementation and MDA measurements with exercise(21,40). The data from this investigation indicate that vitamin E supplementation can decrease the amount of membrane disruption that occurs as a result of increased free radical production. Each group in this investigation had a creatine kinase response similar to that reported in previous studies (5,6). The creatine kinase responses observed in this study indicate that vitamin E had an effect on attenuating the amount of muscle damage that occurred as a result of the resistance exercise protocol. The vitamin E status of our subjects was not measured before or after the supplementation period, but the effectiveness of our supplementation protocol is supported by prior research. A study by Hartmann et al. (16) has already shown that serum alpha-tocopherol concentrations significantly increase with a supplement dose of 1200 mg of vitamin E per day for 14 d in human subjects. Hidiroglou et al.(17) showed a highly significant correlation between plasma alpha-tocopherol levels and muscle tissue levels in animals after supplementation. Meydani et al. (29) have also shown that vitamin E supplementation of 800 IU dL-alpha-tocopherol for 48 d significantly increased alpha-tocopherol levels in human skeletal muscle. In addition, a significant linear increase in tissue alpha-tocopherol levels with progressively increasing amounts of vitamin E intake was reported in as little as 3 d with pigs (1). The previous literature, especially Hartmann et al. (16) and Hidiroglou et al.(17), point to the obvious effectiveness of the supplementation protocol used in this investigation for significantly increasing both plasma and muscle tissue alpha-tocopherol measurements. Additional studies (18,43) support both a linear dose relationship with muscle tissue alpha-tocopherol levels and the effectiveness of these increased levels in suppressing lipid peroxidation in that tissue.

Based on previous investigations it was determined that the intensity of the exercise protocol used is a primary factor in creating a physiological environment for increased free radical production(20,21,26,35-37). The intensity in this investigation was determined by the amount of weight used for each set of each exercise in the protocol. This was expressed in terms of a percentage of each group's 1RM. The intensity was also reported in terms of a 10RM for every set in the exercise protocol. Our data indicate that the resistances used in combination with the selected rest periods created a physiological stress for our subjects that was conducive to an increase in free radical formation. As previously mentioned, studies involving aerobic-type exercise have reported similar findings to this study concerning increases in free radical production with exercise. Hyperoxia at the site of the mitochondria may be a more prominent mechanism for free radical formation during aerobic-type exercise (39). In contrast, intense muscle contractions associated with resistance exercise could result in ischemia-reperfusion at the site of the active muscle. The role of free radicals as mediators of ischemia-reperfusion injury to skeletal muscle and the effectiveness of antioxidants in suppressing the amount of damage to cellular membranes has already been shown in one animal model(38). Another investigation involving canines found that ischemia-reperfusion resulted in muscle injury and was accompanied by increased amounts of free radicals and creatine kinase(4). Several clinical studies have also indicated the involvement of free radicals in ischemia-reperfusion injury in humans(6,11,12). One common mechanism that may exist for both modes of exercise is ischemia-reperfusion injury to some internal organs, such as the liver (24). Further investigation is needed to determine what mechanism(s) are operational. However, ischemia-reperfusion during resistance exercise at the site of the muscle and postexercise production of free radicals via the oxidative burst from neutrophils are realistic concepts that must be seriously considered(22,25,31,33,38,42).

It is now clear that high intensity whole body resistance exercise can result in the formation of free radicals. These free radicals may play a role in how muscle tissue adapts to the physiological stress caused by resistance exercise. Vitamin E is effective in decreasing the amount of muscle membrane disruption that accompanies this type of exercise protocol. This information is a foundation for future investigations into the relationship between free radicals, vitamin E supplementation, and muscle tissue remodeling.

We wish to thank a dedicated group of subjects and members of our clinical and scientific laboratory staffs for their dedication to the project.

This study was supported in part by a grant from the Robert F. and Sandra M. Leitzinger Research Fund in Sports Medicine at The Pennsylvania State University and to Twin Laboratories, Inc., Ronkonkoma, NY for the donation of the supplement and placebo.

Address for correspondence: William J. Kraemer, Ph.D., Professor of Applied Physiology/Director, Laboratory for Sports Medicine, 21 REC Building, The Pennsylvania State University, University Park, PA 16802. E-mail:wjk3@psu.edu.

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Keywords:

MUSCLE DAMAGE; CREATINE KINASE; VITAMINE E; MALONDIALDEHYDE; LIPID PEROXIDATION

©1998The American College of Sports Medicine

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