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Effects of number of eccentric muscle actions on first and second bouts of eccentric exercise of the elbow flexors
Journal of Science and Medicine in Sport (2006) 9, 57—66
ORIGINAL PAPER
Effects of number of eccentric muscle actions on first and second bouts of eccentric exercise of the elbow flexors T.C. Chen a,∗, K. Nosaka b a b
Department of Physical Education, National Chiayi University, Chiayi County, Taiwan School of Exercise, Biomedical and Health Sciences, Edith Cowan University, WA, Australia KEYWORDS Maximal isometric force; Range of motion; Delayed onset muscle soreness (DOMS); Creatine kinase (CK)
Summary This study compared changes in indirect markers of muscle damage following eccentric exercise of the elbow flexors among the exercises consisting of different number of eccentric actions. Sixty male athletes were placed into one of the six groups (n = 10 per group) based on the number of eccentric actions for the first (ECC1) and second exercise bouts (ECC2). Single bout groups (30, 50, and 70) performed ECC1 only, and repeated bout groups (30—30, 50—50, and 70—70) performed ECC2 3 days after ECC1. Another 10 male athletes performed different number of eccentric actions for ECC1 (30) and ECC2 (70) separated by 3 days (30—70). Changes in maximal isometric strength (MVC), range of motion (ROM), upper arm circumference (CIR), serum creatine kinase activity, myoglobin, and nitric oxide concentrations and muscle soreness for 10 days following ECC1 were compared among groups by two-way repeated measures ANOVA. Changes in MVC, ROM, and CIR following ECC1 were significantly (P < 0.05) smaller for the groups that performed 30 eccentric actions compared with other groups. No significant differences between 30 and 30—30, 50 and 50—50, and 70 and 70—70 were evident for the changes in the measures for 10 days following ECC1 except for the acute decreases in MVC and ROM immediately after ECC2 for the repeated bout groups. The 30—30 and 30—70 groups showed similar changes in all criterion measures. It is concluded that recovery from eccentric exercise is not retarded by the second bout of eccentric exercise regardless of the number of eccentric actions. © 2006 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
Introduction
∗
Correspondence to: Department of Physical Education, National Chiayi University, 85 Wenlong Tsuen, Mingsuin Shiang, Chiayi County 621, Taiwan. Tel.: +886 5 226 3411x3015; fax: +886 5 206 3082. E-mail address: [email protected] (T.C. Chen).
It is well documented that eccentric exercise confers adaptation, which is often referred to as repeated bout effect by which indices of muscle damage are attenuated in the subsequent bouts.1 The repeated bout effect has been reported to last for several weeks to several months when the sec-
1440-2440/$ — see front matter © 2006 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.jsams.2006.03.012
58 ond bout of the same exercise is performed after the muscle is presumed to have recovered from the initial bout.1—3 A reduced number of eccentric actions in the first bout can still confer the repeated bout effect. For example, 24 maximal eccentric actions of the elbow flexors (24ECC) rendered protection against 70ECC performed 2 weeks later,4 and the magnitude of muscle damage following 24ECC was attenuated when 2ECC or 6ECC were performed 2 weeks prior to the 24ECC bout.5 Several studies have shown that repeating the same eccentric exercise 2—3 days after the initial bout does not exacerbate muscle damage nor retard the recovery process.6—8 This is also regarded as a repeated bout effect,1,2,5 but this type of repeated bout effect should be considered separately from the case of longer interval (>7 days) between bouts, because responses to the initial bout are still in progress when the second bout is performed. Chen9 showed that 70ECC performed 3 days after 30ECC did not exacerbate muscle damage nor retard recovery, and speculated the existence of a neural inhibitory mechanism. It is also possible that the less forces generated during the second bout are the main reason for the less damage in the repeated exercise bout within 2—3 days after the initial bout. In fact, the previous study9 reported that force output during the second bout of maximal isokinetic eccentric exercise was approximately 50% of the first bout. It is necessary to confirm the repeated bout effect of short interval between bouts by setting a similar intensity of exercise between bouts. To equate the force level and work between bouts separated by 2—3 days as much as possible, it would appear that ‘‘submaximal’’ eccentric exercise using a fixed weight is better, because it gives the muscle constant load, and the work performed is supposed to be similar if the velocity of movement is similar between bouts. Moreover, this type of exercise appears to be more applicable to the situation occurring in actual resistance training than ‘‘maximal’’ isokinetic eccentric exercise. However, no study has used a fixed weight to investigate the effect of initial eccentric exercise bout on the second bout that is performed 3 days later. The present study used an eccentric exercise with a dumbbell to investigate the short interval repeated bout effect. It has been reported that the number of muscle actions in eccentric exercise influences the extent of muscle damage.5,10 However, no study has compared systematically eccentric exercise consisting of different number of eccentric actions for changes in indices of muscle damage following initial and secondary bouts of exercise separated by 3 days. Therefore, the present study was designed
T.C. Chen, K. Nosaka to compare the effect of the three different numbers of eccentric actions (30, 50, and 70) on the initial and repeated bouts of the same number of eccentric actions performed 3 days later using a dumbbell. To confirm the finding of the previous study,9 another group of subjects who performed 30 eccentric actions for the first bout and 70 eccentric actions for the second bout was also included. Additionally, nitric oxide (NO) is known to be associated with vasodilation, inhibition of platelet aggregation, immune function, cell growth, neurotransmission, metabolic regulation, and the excitation—contraction (E—C) coupling.11 Increased NO production by inducible NO synthase (iNOS), expressed during sepsis, has been implicated in animal skeletal muscle dysfunction.12,13 It has been shown that NO reacts with the hydroperoxyl anion (HOO—) to form peroxynitrite,14 which causes cell membrane damage through cytotoxic actions of neutrophils and macrophages as well as the production of peroxynitrite and its derivatives.15 It has been recently suggested that NO plays a role in recovery of skeletal muscle from eccentric exercise.16 It may be that NO concentration in the blood changes as a result of eccentric exercise-induced muscle damage; however, no study has measured serum NO concentration after eccentric exercise. Therefore, the secondary aim of this study was to examine changes in blood NO concentration following the initial and secondary bouts of eccentric exercise consisting of different number of eccentric actions.
Methods Subjects Seventy male students participated in this study that had been approved by the Institutional Ethics Committee, and gave an informed consent form in conformity with the Declaration of Helsinki. All participants were athletes and had been performing their specified sport such as soccer, swimming, shooting, and track and field for 7—10 consecutive years and trained generally at least 5 days (≈14 h) a week. In their regular training, they had resistance training two to three times a week for pre-season, and once a week for in-season. This study was conducted in their off-season, at least 1 month after the last training session, and all subjects were requested not to perform any unaccustomed exercises or vigorous physical activities during the experimental period. They were also asked not to take anti-inflammatory drugs or nutritional supplements during the study.
Effects of number of eccentric muscle actions on ECC1 and ECC2 Table 1
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Physical characteristics of subjects in seven groups
Group
Age (years)
30 50 70 30—30 30—70 50—50 70—70
21.5 21.3 20.9 21.0 21.1 21.6 21.7
± ± ± ± ± ± ±
2.3 2.4 2.0 2.1 2.2 2.3 2.4
Height (cm) 173.5 173.1 173.0 173.1 173.3 173.1 172.9
± ± ± ± ± ± ±
6.7 6.1 6.4 6.0 6.5 6.2 5.8
Weight (kg) 63.8 63.5 64.1 63.3 63.0 64.0 63.9
± ± ± ± ± ± ±
7.1 7.0 7.8 7.3 7.0 7.7 7.5
MVC (kg) 27.9 27.5 27.8 27.4 27.6 27.3 27.8
± ± ± ± ± ± ±
3.9 3.4 3.6 3.0 3.4 2.9 3.1
Values are represented as means ± S.D. No significant differences between the groups.
Based on the baseline maximal isometric strength of the elbow flexors (MVC) at the elbow joint of 90◦ , subjects were placed into six groups by equating the average pre-exercise MVC among the groups. The groups were made based on the number of eccentric actions for the first bout; 30 (n = 20), 50 (n = 20), or 70 (n = 20) group, then each group was subdivided into two groups (n = 10 for each group) according to the number of exercise bouts; single (30, 50, and 70) or repeated bout group (30—30, 50—50, and 70—70). Additionally, a group of subjects (n = 10) was set to examine the effect of 30 eccentric actions that were performed in the first bout on the subsequent bout of 70 eccentric actions 3 days later to confirm the findings of the previous study9 showing that a repeated bout of 70ECC 3 days after the initial 30ECC did not exacerbate muscle damage nor retarded the recovery process. No significant differences in age, height, weight and MVC among the groups were evident (Table 1).
Eccentric exercise protocol For the initial bout (ECC1), participants that performed either 30, 50, or 70 eccentric actions of the elbow flexors of the non-dominant arm using a dumbbell that was set at 80% of each subject’s MVC at the elbow angle of 90◦ (1.57 rad). This load was chosen because it is commonly used in a weight-training program,17 and our pilot study had shown that subjects could perform the second bout of eccentric exercise of the same weight in a reasonably similar fashion to the initial bout in 3-day intervals. The average dumbbell weight was 22.0 ± 3.8 kg without significant differences among the groups. Three days after ECC1, subjects in the 30—30, 30—70, 50—50, and 70—70 groups repeated the second bout (ECC2) consisting of 30, 70, 50, and 70 eccentric actions, respectively, using the same dumbbell used in ECC1. For each eccentric action, subjects were asked to lower the dumbbell from an elbow flexed (50◦ , 0.87 rad) to an elbow extended
position (170◦ , 2.97 rad) in 4—5 s. After completing each eccentric action, the examiner removed the dumbbell at the elbow extended position, and the subjects returned the arm to the flexed position without load and rested for 45 s between actions. Subjects were verbally encouraged to maximally resist against the action throughout the range of motion, and the examiner instructed the participants to control the lowering velocity of the dumbbell by counting ‘‘0’’ for the beginning and ‘‘1, 2, 3, 4, and 5’’ for the movement.
Criterion measures MVC and active range of motion (ROM) were measured before and immediately after ECC1 and ECC2, and every 24 h for 10 consecutive days following ECC1. Muscle soreness, upper arm circumference (CIR), serum creatine kinase (CK) activity, and myoglobin (Mb) concentration were assessed before and every 24 h for 10 consecutive days after ECC1. Serum nitric oxide concentration was measured for the same time course as CK and Mb for all groups but the 30—70 group. To check the reliability of the measurements of MVC, ROM, and CIR, the measurements were also taken 2 days before ECC1, and compare to the values of immediately before ECC1. The intraclass correlation coefficient (r) values for MVC, ROM, and CIR were 0.96, 0.90, and 0.98, respectively.
MVC MVC was recorded for 3 s at the elbow angle of 90◦ (1.57 rad) on a modified arm curl machine using a force transducer (Model DFG51, Omega Systems, Inc., Stamford, CT, USA) connected to a digital recorder (Model MP100, Biopac Systems, Inc., Goleta, CA, USA). Although it has been documented that muscle damage from unaccustomed eccentric exercise results in a significant rightward shift of the muscle’s length—tension relationship,18,19 the present study chose a fixed angle (90◦ ) as previ-
60 ous studies did.2,9 Three trials were performed with 1-min rest between each contraction, and the average of the peak of three trials was used for further analysis.9
Elbow joint angles and ROM Flexed (FANG) and relaxed (RANG) elbow joint angles were measured three times for each time point using a goniometer (Creative Health Products, Plymouth, MI, USA). FANG was the angle when the subjects tried to fully flex the elbow joint to touch the shoulder by the palm while keeping the elbow at the side. RANG was the angle where the subjects relaxed the arm allowing it to hang down by the side. A semipermanent marker was used to identify the landmarks such as the lateral centre point of the humerus, the lateral centre point of elbow joint and the lateral centre point between radius and ulna for the goniometer placements. ROM was calculated by subtracting FANG from RANG.6,9
CIR CIR was measured three times at 8 cm above the elbow joint with a Gulick tape measure while allowing the arm hang down by the side of the body.9 This point was marked on the subject’s arm to ensure consistent placement of the tape measure, and the mean value of the three measurements was used for the analysis.
Muscle soreness Muscle soreness was evaluated using a visual analogue scale of a 100-mm continuous line that represents ‘‘no sore’’ at one side (0 mm) and ‘‘very, very sore’’ at the other side (100 mm). Subjects were asked to report the soreness level on the line when an investigator palpated over the biceps brachii and extended the elbow.9
T.C. Chen, K. Nosaka Nucleonics, Fairfield, NJ, USA) using a test kit (Sigma Diagnostics, St. Louis, MO, USA). Serum Mb concentration was measured by a biochemical analyser (Model ADVIA-Centaur, Bayer Co. Ltd., Germany) using a test kit (Denka-Seiken Co. Ltd., Japan). All samples were analysed in duplicate, and the mean of the two measures was used for subsequent statistical analysis. NO concentration was determined by an enzyme-linked immunosorbent assay (ELISA; Model ELX 800, BioTek, Burlington, VA, USA) using a kit (R&D Minneapolis, MN, USA). The normal reference ranges for CK, Mb, and NO were 38—174 IU L−1 , <110 g L−1 , and <12.8 mM L−1 , respectively.
Statistical analysis Changes in the criterion measures over time were compared among the single bout groups (30, 50, 70) and among the repeated bout groups (30—30, 50—50, 70—70) separately by two-way repeated measures ANOVA (30 versus 50, 30 versus 70, 50 versus 70, 30—30 versus 50—50, 30—30 versus 70—70, and 50—50 versus 70—70) were performed by twoway repeated measures ANOVA. To examine the effects of ECC2, changes in the criterion measures over time were compared between 30 and 30—30, 50 and 50—50, and 70 and 70—70 groups by two-way repeated measures ANOVA. Comparison between 30—70 and 70—70 groups were also made by twoway repeated measures ANOVA to examine if the 30 eccentric actions performed in the ECC1 had the same effects on ECC2 (70 eccentric actions) as the protocol in which 70 eccentric actions were performed in ECC1. When the ANOVA found a significant interaction (group × time) effect, a Sheff´ e’s post hoc test was conducted to specify the time points where significant differences were evident. Statistical significance was set at P < 0.05. Unless otherwise stated, data are presented as means ± S.D.
Results Blood markers Exercise All subjects visited the laboratory in the morning, and a 10 mL venous blood sample was collected by venipuncture from the cubital fossa region of the dominant arm. The blood was allowed to clot for 30 min at room temperature and centrifuged for 10 min to obtain serum. Serum samples were stored at −20 ◦ C until analysis for CK activity, Mb, and NO concentrations. Serum CK activity was determined spectrophotometrically by a Genstar chemistry analyser (Electro-
All subjects were able to perform the exercise without spotting even for ECC2 that was performed with muscles demonstrated lower MVC compared to the pre-ECC1 level (Fig. 1). However in ECC2, some subjects had difficulty in lowering the dumbbell slowly for extended elbow joint angles (140—170◦ ) and needed to spend a longer time before reaching to the weak angles to keep the eccentric action time for 4—5 s.
Effects of number of eccentric muscle actions on ECC1 and ECC2
61
Figure 1 Changes in MVC (upper two graphs: a and b) and ROM (lower two graphs: c and d) over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a and c) and 30—30, 50—50, 70—70, and 30—70 groups (b and d). Changes in MVC immediately after ECC2 are shown for the groups performed ECC2 (30—30, 30—70, 50—50, and 70—70). Asterisk (*) indicates a significant (P < 0.05) difference between groups. On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
MVC Comparisons among 30, 50, 70 groups, and among 30—30, 50—50, and 70—70 groups, showed that decreases in MVC after ECC1 were significantly smaller (P < 0.05) for 30 eccentric actions compared to 50 and 70 eccentric actions (Fig. 1). MVC recovered to baseline by 10 days after ECC1 for the groups that performed 30 eccentric actions in ECC1, but MVC was not fully recovered at 10 days post-ECC1 for other groups. No significant differences between 50 and 70 groups (P = 0.24), and 50—50 and 70—70 groups (P = 0.26) were evident for the changes in MVC following ECC1. Immediately after ECC2, MVC decreased significantly (P < 0.05) for the 30—30 (5.3%), 30—70 (12.5%), 50—50 (8.2%), and 70—70 (9.1%) groups, and the magnitude of decrease in MVC for the 30—30 was significantly (P < 0.05) smaller than other groups. Despite the decrease in MVC immediately post-
ECC2, MVC recovered to pre-ECC2 level by next day, and no significant differences between 30 and 30—30 (P = 0.31), 50 and 50—50 (P = 0.26), and 70 and 70—70 groups (P = 0.17) were evident. Changes in MVC after ECC2 were not significantly (P = 0.91) different between 30—30 and 30—70 groups.
ROM ROM decreased significantly (P < 0.05) immediately following ECC1, and did not recover for the next 2 days, but started to recover after 3 days postexercise for all groups (Fig. 1). The decreases in ROM after ECC1 were significantly (P < 0.05) smaller for 30 eccentric actions compared to 50 and 70 eccentric actions. No significant differences between 50 and 70 groups (P = 0.78), and 50—50 and 70—70 groups (P = 0.67) were evident
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T.C. Chen, K. Nosaka
Figure 2 Changes in upper arm circumference over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a) and 30—30, 50—50, 70—70, and 30—70 groups (b). Asterisk (*) indicates a significant (P < 0.05) difference between groups. On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
for the changes in ROM following ECC1. Immediately after ECC2, a significant (P < 0.05) decrease in ROM was evident for the 30—30 (22.6◦ ), 30—70 (26.6◦ ), 50—50 (27.9◦ ), and 70—70 (31.4◦ ) groups, and the magnitude of decrease in ROM for the 30—30 was significantly (P < 0.05) smaller than that of other groups. ROM recovered to pre-ECC2 level by next day after ECC2, and no significant differences between 30 and 30—30 (P = 0.23), 50 and 50—50 (P = 0.10), and 70 and 70—70 groups (P = 0.12) were evident. Changes in ROM after ECC2 were not
significantly (P = 0.56) different between 30—30 and 30—70 groups.
CIR Significant increases in CIR were observed following ECC1 for all groups, and CIR peaked 5—8 days after exercise with 10—13 mm increase from the baseline (Fig. 2). The groups that performed 30 eccentric actions for the first bout (30, 30—30) showed significantly (P < 0.05) smaller increases in CIR fol-
Figure 3 Changes in muscle soreness over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a) and 30—30, 50—50, 70—70, and 30—70 groups (b). On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
Effects of number of eccentric muscle actions on ECC1 and ECC2 lowing ECC1 compared with other groups. No significant differences between 50 and 70 (P = 0.49), and 50—50 and 70—70 (P = 0.30) were seen. No significant (P = 0.93) difference between 30—30 and 30—70 groups was evident for changes in CIR following ECC1.
Muscle soreness Muscle soreness developed significantly (P < 0.05) 1 day after ECC1, peaked 1—3 days, and lasted for 7 days following ECC1 for all groups. No significant differences among the single bout (30, 50, 70) (P = 0.53) and repeated bout (30—30, 50—50, 70—70) groups (P = 0.35) were evident for the changes in muscle soreness following ECC1 (Fig. 3). Changes in muscle soreness were not significantly (P = 0.62) different between 30—30 and 30—70 groups following ECC1.
63
CK, Mb, and NO Serum CK activity and Mb concentration showed significant (P < 0.05) increases at 3 days after ECC1, peaked 4—6 days, and still elevated from the baseline at 10 days after ECC1 for all groups (Fig. 4). Changes in serum CK activity and Mb concentration were not significantly different among the single bout (30, 50, 70) (P = 0.07 for CK and P = 0.21 for Mb) and repeated bout (30—30, 50—50, 70—70) (P = 0.13 for CK and P = 0.34 for Mb) groups following ECC1. Serum NO concentration increased significantly (P < 0.05) 1—4 days after ECC1 for all groups, but no further increases in NO were observed after ECC2 for all groups (Fig. 5). No significant differences between the single bout (30, 50, 70) (P = 0.16) and repeated bout (30—30, 50—50, 70—70) groups (P = 0.11) were observed following ECC1.
Figure 4 Changes in plasma CK activity (upper two graphs: a and b) and myoglobin concentration (lower two graphs: c and d) over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a and c) and 30—30, 50—50, 70—70, and 30—70 groups (b and d). On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
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T.C. Chen, K. Nosaka
Figure 5 Changes in serum NO concentration over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a) and 30—30, 50—50, and 70—70 groups (b). On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
Discussion The originality of the present study was the use of dumbbell for the two bouts of eccentric exercise, and compared among 30, 50, 70 eccentric actions for changes in common markers of muscle damage and NO following single and repeated exercise bouts. The main findings of this study were that: (1) decreases in MVC and ROM, and increases in CIR following ECC1 were significantly smaller for the groups that performed 30 eccentric actions compared to the groups that performed 50 or 70 eccentric actions, and (2) ECC2 performed 3 days after ECC1 did not affect the changes in all criterion measures following ECC1 regardless of the number of eccentric actions. These results confirm the previous studies reporting that a repeated bout of eccentric exercise performed in early recovery days after the initial eccentric exercise does not induce further damage nor retard the recovery6—8 even if more strenuous exercise is performed 3 days after the initial bout.9 One previous study9 used isokinetic eccentric exercise and reported that 70 maximal eccentric actions (70ECC) performed 3 days after 30 maximal eccentric actions (30ECC) did not exacerbate damage nor retard recovery. However, the force generated during 30 or 70 maximal isokinetic eccentric actions in the previous study was approximately 50% lower in the second bout compared to the first bout. This suggests that the second bout was not as strenuous as the first bout in the previous study. In contrast, the present study used the same dumbbell load for the first and second bouts of exercise, and
subjects made maximal effort to perform the second bout similarly to the first bout. Although some subjects had difficulty in lowering the dumbbell slowly for extended elbow joint angles and needed to spend a longer time before reaching to the weak angles, it would appear that the total work of the exercise was similar between bouts, because the weight, movement range, and the time when muscles were activated were the same between bouts. When comparing between the dumbbell exercise in the present study and the isokinetic exercise in the previous study,9 the decreases in MVC and ROM, and the increases in CIR and CK, were greater following the isokinetic exercise than after the dumbbell exercise. This suggests that the dumbbell eccentric exercise was less strenuous than the isokinetic eccentric exercise for the first bout. However, it seems likely that the second bout in the present study was more strenuous than the second bout using the isokinetic exercise in the previous study.9 It is interesting to note that all subjects in the repeated bout group (30—30, 30—70, 50—50, and 70—70) were able to perform ECC2 without spotting, although the MVC immediately prior to ECC2 was significantly lower than that before ECC1 (Fig. 1). It would appear that eccentric force generation is maintained when isometric force (measured 90◦ elbow angle) is reduced. Since the MVC before ECC2 was lower than that before ECC1, it seems that exercise stress induced by ECC2 was larger than that by ECC1, and the dumbbell exercise was more strenuous than the isokinetic exercise for the second bout. However, the findings were not different from those in previous studies.6,9 This suggests
Effects of number of eccentric muscle actions on ECC1 and ECC2 that muscles recovering from the initial damage are not affected by a subsequent exercise bout regardless of the intensity and volume of the exercise bout. Changes in MVC (Fig. 1), ROM (Fig. 1), and CIR (Fig. 2) following ECC1 were significantly smaller following 30 eccentric actions compared to 50 or 70 eccentric actions, and no significant differences between 50 and 70 eccentric actions were found. Moreover, no significant differences among the groups were found for muscle soreness (Fig. 3), serum CK activity (Fig. 4), Mb (Fig. 4), and NO concentrations (Fig. 5). These results suggest that the effect of number of eccentric action was minor, at least among 30, 50, and 70 eccentric actions of the elbow flexors. It may be that muscle fatigue was caused more in the 50 and 70 eccentric actions, and the decrease in ability to produce high force reduced mechanical stress to the muscles. The mechanisms to explain why recovering muscles from eccentric exercise do not suffer from the additional bout of eccentric exercise are unclear. As shown in the present study and previous studies,6—8 it appears that damaged muscle is protected against further damaging stimulus. It has been reported that regeneration of damaged tissue after eccentric exercise takes more than a week.20,21 Considering the short time between ECC1 and ECC2, it seems unlikely that muscle fibres become more resilient in the 3 days after the initial bout. It has been speculated that a population of stress-susceptible fibres is eliminated in the initial bout.1,22 This may explain better the phenomenon of protective effect in a short interval between bouts. It is also reported that optimal angle to generate maximal force shifts to a long muscle length after eccentric exercise18,19 and this is postulated as a mechanism of the repeated bout effect.19 This theory also fits to the short interval repeated bout effect. A recent work9 showed that activation of fast-twitch motor units were reduced in the second bout, and suggested a neural protective mechanism. Further study is necessary to investigate the underlying mechanisms of the repeated bout effect. Serum NO concentration increased significantly by 40% from the baseline 1 and 2 days after ECC1, and elevated for 4 days post-exercise (Fig. 5). To our knowledge, this is the first study to report changes in serum NO concentration after eccentric exercise. It should be noted that the time course of changes in NO were different from that of CK and Mb (Fig. 4), which did not returned to the baseline by 10 days post-exercise. This would suggest that the mechanism of increase in NO is different from that of CK and Mb. Rad´ ak et al.23 reported that NO content
65
in human skeletal muscle increased significantly by 25% at 24 h after 200 eccentric muscle actions of the rectus femoris. The authors suggested that the activation of iNOS in the damaged muscle fibres or activated macrophages in the site of muscle damage was associated with the increase in NO content in the muscle after eccentric exercise.23 It is postulated that increases in blood NO indicate an inflammatory response.15,24 As eccentric exerciseinduced muscle damage also consists of inflammatory responses,2,15,25 the increases in serum NO concentration may reflect inflammation. It has been reported that inflammatory responses last longer than 4 days after eccentric exercise, and usually become more pronounced in the late recovery process in eccentric exercise-induced muscle damage.2,26 However, serum NO concentration showed a largest increase at 1—2 days post-ECC1, and returned to baseline when swelling was most conspicuous (Fig. 2). It would appear that serum NO concentration does not involve in the inflammatory responses after eccentric exercise directly. Further study is necessary to understand the physiological significance of blood NO concentration, and what caused the increase in serum NO after eccentric exercise. In summary, the results of the present study confirmed that repeated eccentric exercise bout performed in early recovery days from initial eccentric exercise did not induce further muscle damage nor retard the recovery process regardless the intensity and volume of eccentric actions performed in the repeated bout. This suggests that muscles recovering from eccentric exercise-induced muscle damage are not affected by additional eccentric exercise; however, the underlying mechanisms are still unknown.
Practical implications • The results of our study confirmed that repeated eccentric exercise bout performed in early recovery days from initial eccentric exercise do not induce further muscle damage nor retard the recovery process regardless of the intensity and volume of eccentric actions in the repeated bout exercise. • They suggest that athletes can perform high volume resistance training at least every 3 days without considering any adverse effects on muscle function and pain sensation. This has confirmed the notion that delayed onset muscle soreness can be ignored, and training with sore muscles does not affect recovery
66 of muscle damage with a minimal chance to suffer from further muscle damage, though it is important to differentiate between eccentric exercise-induced muscle damage and muscle strains/soft tissue injury. • If muscle pain is associated with the injury, an additional bout may be detrimental. Strength coaches and trainers should examine the cause of muscle pain carefully.
References 1. McHugh MP, Connolly DAJ, Eston RG, et al. Exercise-induced muscle damage and potential mechanisms for the repeated bout effect. Sports Med 1999;27:157—70. 2. Clarkson PM, Nosaka K, Braun B. Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 1992;24:512—20. 3. Nosaka K, Sakamoto K, Newton M, et al. The repeated bout effect of reduced-load eccentric exercise on elbow flexor muscle damage. Eur J Appl Physiol 2001;85:34— 40. 4. Clarkson PM, Tremblay I. Rapid adaptation to exerciseinduced muscle damage. J Appl Physiol 1988;65:1—6. 5. Nosaka K, Sakamoto K, Newton M, et al. How long does the protective effect on eccentric exercise-induced muscle damage last? Med Sci Sports Exerc 2001;33: 1490—5. 6. Chen TC, Hsieh SS. The effects of repeated maximal isokinetic eccentric exercise on recovery from muscle damage. Res Q Exerc Sport 2000;71:260—6. 7. Paddon-Jones D, Mathalib D, Jenkins D. The effect of a repeated bout of eccentric exercise on induces of muscle damage and delayed onset muscle soreness. J Sci Med Sport 2000;3(3):35—43. 8. Smith LL, Fulmer MG, Holbert D, et al. The impact of a repeated bout of eccentric exercise on muscular strength, muscle soreness and creatine kinase. Br J Sports Med 1994;28:267—71. 9. Chen TC. Effects of a second bout of maximal eccentric exercise on muscle damage and EMG activity. Eur J Appl Physiol 2003;89:115—21. 10. McCully KK, Faulkner JA. Characteristics of lengthening contractions associated with injury to skeletal muscle fibers. J Appl Physiol 1986;61:293—9.
T.C. Chen, K. Nosaka 11. Kingwell BA. Nitric oxide-metabolic regulation during exercise: effects of training in health and disease. FASEB J 2000;14(12):1685—96. 12. Gath I, Closs EI, G¨ odtel-Armbrust U, et al. Inducible NO synthase II and neuronal NO synthase I are constitutively expressed in different structures of guinea pig skeletal muscle: implications for contractile function. FASEB J 1996;10(14):1614—20. 13. Krause KM, Moody MR, Andrade FH, et al. Peritonitis causes diaphragm weakness in rats. Am J Respir Crit Care Med 1998;157:1277—82. 14. Koppenol WH. The chemical reactivity of radicals. In: Wallace KB, editor. Free radical toxicology. Washington, DC: Taylor & Francis; 1997 [chapter 1]. 15. Pyne DB. Exercise-induced muscle damage and inflammation: a review. Aust J Sci Med 1994;26:49—58. 16. Sakurai T, Hollander J, Brickson SL, et al. Changes in nitric oxide and inducible nitric oxide synthase following stretchinduced injury to the tibialis anterior muscle of rabbit. Jpn J Physiol 2005;55(2):101—7. 17. Dons V, Bollerup K, Bonde-Peterson F, et al. The effect of weight-lifting exercise related to muscle fiber composition and muscle cross-sectional area in humans. Eur J Appl Physiol 1979;40:95—106. 18. Proske U, Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 2001;537:333—45. 19. Brockett CL, Morgan DL, Proske U. Human hamstring muscles adapt to eccentric exercise by changing optimum length. Med Sci Sports Exerc 2001;33:783—90. 20. Frid´ en J, Sj¨ ostr¨ om M, Ekblom B. A morphological study of delayed muscle soreness. Experientia 1981;37:506—7. 21. Frid´ en J, Sj¨ ostr¨ om M, Ekblom B. Myofibrillar damage following intensive eccentric exercise in man. Int J Sports Med 1983;4:170—6. 22. Armstrong RB. Muscle damage and endurance events. Sports Med 1986;3:370—81. 23. Rad´ ak Z, Pucsok J, Mecseki S, et al. Muscle sorenessinduced reduction in force generation is accompanied by increased nitric oxide content and DNA damage in human skeletal muscle. Free Radic Biol Med 1999;26:1059—63. 24. Node K, Kitakaze M, Sato H, et al. Increased release of nitric oxide in ischemic hearts after exercise in patients with effort angina. J Coll Cardiol 1998;32:63—8. 25. Smith LL. Acute inflammation: the underlying mechanism in delayed onset muscle soreness? Med Sci Sports Exerc 1991;23(5):542—51. 26. Nosaka K, Clarkson PM. Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med Sci Sports Exerc 1996;28:953—61.
ORIGINAL PAPER
Effects of number of eccentric muscle actions on first and second bouts of eccentric exercise of the elbow flexors T.C. Chen a,∗, K. Nosaka b a b
Department of Physical Education, National Chiayi University, Chiayi County, Taiwan School of Exercise, Biomedical and Health Sciences, Edith Cowan University, WA, Australia KEYWORDS Maximal isometric force; Range of motion; Delayed onset muscle soreness (DOMS); Creatine kinase (CK)
Summary This study compared changes in indirect markers of muscle damage following eccentric exercise of the elbow flexors among the exercises consisting of different number of eccentric actions. Sixty male athletes were placed into one of the six groups (n = 10 per group) based on the number of eccentric actions for the first (ECC1) and second exercise bouts (ECC2). Single bout groups (30, 50, and 70) performed ECC1 only, and repeated bout groups (30—30, 50—50, and 70—70) performed ECC2 3 days after ECC1. Another 10 male athletes performed different number of eccentric actions for ECC1 (30) and ECC2 (70) separated by 3 days (30—70). Changes in maximal isometric strength (MVC), range of motion (ROM), upper arm circumference (CIR), serum creatine kinase activity, myoglobin, and nitric oxide concentrations and muscle soreness for 10 days following ECC1 were compared among groups by two-way repeated measures ANOVA. Changes in MVC, ROM, and CIR following ECC1 were significantly (P < 0.05) smaller for the groups that performed 30 eccentric actions compared with other groups. No significant differences between 30 and 30—30, 50 and 50—50, and 70 and 70—70 were evident for the changes in the measures for 10 days following ECC1 except for the acute decreases in MVC and ROM immediately after ECC2 for the repeated bout groups. The 30—30 and 30—70 groups showed similar changes in all criterion measures. It is concluded that recovery from eccentric exercise is not retarded by the second bout of eccentric exercise regardless of the number of eccentric actions. © 2006 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
Introduction
∗
Correspondence to: Department of Physical Education, National Chiayi University, 85 Wenlong Tsuen, Mingsuin Shiang, Chiayi County 621, Taiwan. Tel.: +886 5 226 3411x3015; fax: +886 5 206 3082. E-mail address: [email protected] (T.C. Chen).
It is well documented that eccentric exercise confers adaptation, which is often referred to as repeated bout effect by which indices of muscle damage are attenuated in the subsequent bouts.1 The repeated bout effect has been reported to last for several weeks to several months when the sec-
1440-2440/$ — see front matter © 2006 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.jsams.2006.03.012
58 ond bout of the same exercise is performed after the muscle is presumed to have recovered from the initial bout.1—3 A reduced number of eccentric actions in the first bout can still confer the repeated bout effect. For example, 24 maximal eccentric actions of the elbow flexors (24ECC) rendered protection against 70ECC performed 2 weeks later,4 and the magnitude of muscle damage following 24ECC was attenuated when 2ECC or 6ECC were performed 2 weeks prior to the 24ECC bout.5 Several studies have shown that repeating the same eccentric exercise 2—3 days after the initial bout does not exacerbate muscle damage nor retard the recovery process.6—8 This is also regarded as a repeated bout effect,1,2,5 but this type of repeated bout effect should be considered separately from the case of longer interval (>7 days) between bouts, because responses to the initial bout are still in progress when the second bout is performed. Chen9 showed that 70ECC performed 3 days after 30ECC did not exacerbate muscle damage nor retard recovery, and speculated the existence of a neural inhibitory mechanism. It is also possible that the less forces generated during the second bout are the main reason for the less damage in the repeated exercise bout within 2—3 days after the initial bout. In fact, the previous study9 reported that force output during the second bout of maximal isokinetic eccentric exercise was approximately 50% of the first bout. It is necessary to confirm the repeated bout effect of short interval between bouts by setting a similar intensity of exercise between bouts. To equate the force level and work between bouts separated by 2—3 days as much as possible, it would appear that ‘‘submaximal’’ eccentric exercise using a fixed weight is better, because it gives the muscle constant load, and the work performed is supposed to be similar if the velocity of movement is similar between bouts. Moreover, this type of exercise appears to be more applicable to the situation occurring in actual resistance training than ‘‘maximal’’ isokinetic eccentric exercise. However, no study has used a fixed weight to investigate the effect of initial eccentric exercise bout on the second bout that is performed 3 days later. The present study used an eccentric exercise with a dumbbell to investigate the short interval repeated bout effect. It has been reported that the number of muscle actions in eccentric exercise influences the extent of muscle damage.5,10 However, no study has compared systematically eccentric exercise consisting of different number of eccentric actions for changes in indices of muscle damage following initial and secondary bouts of exercise separated by 3 days. Therefore, the present study was designed
T.C. Chen, K. Nosaka to compare the effect of the three different numbers of eccentric actions (30, 50, and 70) on the initial and repeated bouts of the same number of eccentric actions performed 3 days later using a dumbbell. To confirm the finding of the previous study,9 another group of subjects who performed 30 eccentric actions for the first bout and 70 eccentric actions for the second bout was also included. Additionally, nitric oxide (NO) is known to be associated with vasodilation, inhibition of platelet aggregation, immune function, cell growth, neurotransmission, metabolic regulation, and the excitation—contraction (E—C) coupling.11 Increased NO production by inducible NO synthase (iNOS), expressed during sepsis, has been implicated in animal skeletal muscle dysfunction.12,13 It has been shown that NO reacts with the hydroperoxyl anion (HOO—) to form peroxynitrite,14 which causes cell membrane damage through cytotoxic actions of neutrophils and macrophages as well as the production of peroxynitrite and its derivatives.15 It has been recently suggested that NO plays a role in recovery of skeletal muscle from eccentric exercise.16 It may be that NO concentration in the blood changes as a result of eccentric exercise-induced muscle damage; however, no study has measured serum NO concentration after eccentric exercise. Therefore, the secondary aim of this study was to examine changes in blood NO concentration following the initial and secondary bouts of eccentric exercise consisting of different number of eccentric actions.
Methods Subjects Seventy male students participated in this study that had been approved by the Institutional Ethics Committee, and gave an informed consent form in conformity with the Declaration of Helsinki. All participants were athletes and had been performing their specified sport such as soccer, swimming, shooting, and track and field for 7—10 consecutive years and trained generally at least 5 days (≈14 h) a week. In their regular training, they had resistance training two to three times a week for pre-season, and once a week for in-season. This study was conducted in their off-season, at least 1 month after the last training session, and all subjects were requested not to perform any unaccustomed exercises or vigorous physical activities during the experimental period. They were also asked not to take anti-inflammatory drugs or nutritional supplements during the study.
Effects of number of eccentric muscle actions on ECC1 and ECC2 Table 1
59
Physical characteristics of subjects in seven groups
Group
Age (years)
30 50 70 30—30 30—70 50—50 70—70
21.5 21.3 20.9 21.0 21.1 21.6 21.7
± ± ± ± ± ± ±
2.3 2.4 2.0 2.1 2.2 2.3 2.4
Height (cm) 173.5 173.1 173.0 173.1 173.3 173.1 172.9
± ± ± ± ± ± ±
6.7 6.1 6.4 6.0 6.5 6.2 5.8
Weight (kg) 63.8 63.5 64.1 63.3 63.0 64.0 63.9
± ± ± ± ± ± ±
7.1 7.0 7.8 7.3 7.0 7.7 7.5
MVC (kg) 27.9 27.5 27.8 27.4 27.6 27.3 27.8
± ± ± ± ± ± ±
3.9 3.4 3.6 3.0 3.4 2.9 3.1
Values are represented as means ± S.D. No significant differences between the groups.
Based on the baseline maximal isometric strength of the elbow flexors (MVC) at the elbow joint of 90◦ , subjects were placed into six groups by equating the average pre-exercise MVC among the groups. The groups were made based on the number of eccentric actions for the first bout; 30 (n = 20), 50 (n = 20), or 70 (n = 20) group, then each group was subdivided into two groups (n = 10 for each group) according to the number of exercise bouts; single (30, 50, and 70) or repeated bout group (30—30, 50—50, and 70—70). Additionally, a group of subjects (n = 10) was set to examine the effect of 30 eccentric actions that were performed in the first bout on the subsequent bout of 70 eccentric actions 3 days later to confirm the findings of the previous study9 showing that a repeated bout of 70ECC 3 days after the initial 30ECC did not exacerbate muscle damage nor retarded the recovery process. No significant differences in age, height, weight and MVC among the groups were evident (Table 1).
Eccentric exercise protocol For the initial bout (ECC1), participants that performed either 30, 50, or 70 eccentric actions of the elbow flexors of the non-dominant arm using a dumbbell that was set at 80% of each subject’s MVC at the elbow angle of 90◦ (1.57 rad). This load was chosen because it is commonly used in a weight-training program,17 and our pilot study had shown that subjects could perform the second bout of eccentric exercise of the same weight in a reasonably similar fashion to the initial bout in 3-day intervals. The average dumbbell weight was 22.0 ± 3.8 kg without significant differences among the groups. Three days after ECC1, subjects in the 30—30, 30—70, 50—50, and 70—70 groups repeated the second bout (ECC2) consisting of 30, 70, 50, and 70 eccentric actions, respectively, using the same dumbbell used in ECC1. For each eccentric action, subjects were asked to lower the dumbbell from an elbow flexed (50◦ , 0.87 rad) to an elbow extended
position (170◦ , 2.97 rad) in 4—5 s. After completing each eccentric action, the examiner removed the dumbbell at the elbow extended position, and the subjects returned the arm to the flexed position without load and rested for 45 s between actions. Subjects were verbally encouraged to maximally resist against the action throughout the range of motion, and the examiner instructed the participants to control the lowering velocity of the dumbbell by counting ‘‘0’’ for the beginning and ‘‘1, 2, 3, 4, and 5’’ for the movement.
Criterion measures MVC and active range of motion (ROM) were measured before and immediately after ECC1 and ECC2, and every 24 h for 10 consecutive days following ECC1. Muscle soreness, upper arm circumference (CIR), serum creatine kinase (CK) activity, and myoglobin (Mb) concentration were assessed before and every 24 h for 10 consecutive days after ECC1. Serum nitric oxide concentration was measured for the same time course as CK and Mb for all groups but the 30—70 group. To check the reliability of the measurements of MVC, ROM, and CIR, the measurements were also taken 2 days before ECC1, and compare to the values of immediately before ECC1. The intraclass correlation coefficient (r) values for MVC, ROM, and CIR were 0.96, 0.90, and 0.98, respectively.
MVC MVC was recorded for 3 s at the elbow angle of 90◦ (1.57 rad) on a modified arm curl machine using a force transducer (Model DFG51, Omega Systems, Inc., Stamford, CT, USA) connected to a digital recorder (Model MP100, Biopac Systems, Inc., Goleta, CA, USA). Although it has been documented that muscle damage from unaccustomed eccentric exercise results in a significant rightward shift of the muscle’s length—tension relationship,18,19 the present study chose a fixed angle (90◦ ) as previ-
60 ous studies did.2,9 Three trials were performed with 1-min rest between each contraction, and the average of the peak of three trials was used for further analysis.9
Elbow joint angles and ROM Flexed (FANG) and relaxed (RANG) elbow joint angles were measured three times for each time point using a goniometer (Creative Health Products, Plymouth, MI, USA). FANG was the angle when the subjects tried to fully flex the elbow joint to touch the shoulder by the palm while keeping the elbow at the side. RANG was the angle where the subjects relaxed the arm allowing it to hang down by the side. A semipermanent marker was used to identify the landmarks such as the lateral centre point of the humerus, the lateral centre point of elbow joint and the lateral centre point between radius and ulna for the goniometer placements. ROM was calculated by subtracting FANG from RANG.6,9
CIR CIR was measured three times at 8 cm above the elbow joint with a Gulick tape measure while allowing the arm hang down by the side of the body.9 This point was marked on the subject’s arm to ensure consistent placement of the tape measure, and the mean value of the three measurements was used for the analysis.
Muscle soreness Muscle soreness was evaluated using a visual analogue scale of a 100-mm continuous line that represents ‘‘no sore’’ at one side (0 mm) and ‘‘very, very sore’’ at the other side (100 mm). Subjects were asked to report the soreness level on the line when an investigator palpated over the biceps brachii and extended the elbow.9
T.C. Chen, K. Nosaka Nucleonics, Fairfield, NJ, USA) using a test kit (Sigma Diagnostics, St. Louis, MO, USA). Serum Mb concentration was measured by a biochemical analyser (Model ADVIA-Centaur, Bayer Co. Ltd., Germany) using a test kit (Denka-Seiken Co. Ltd., Japan). All samples were analysed in duplicate, and the mean of the two measures was used for subsequent statistical analysis. NO concentration was determined by an enzyme-linked immunosorbent assay (ELISA; Model ELX 800, BioTek, Burlington, VA, USA) using a kit (R&D Minneapolis, MN, USA). The normal reference ranges for CK, Mb, and NO were 38—174 IU L−1 , <110 g L−1 , and <12.8 mM L−1 , respectively.
Statistical analysis Changes in the criterion measures over time were compared among the single bout groups (30, 50, 70) and among the repeated bout groups (30—30, 50—50, 70—70) separately by two-way repeated measures ANOVA (30 versus 50, 30 versus 70, 50 versus 70, 30—30 versus 50—50, 30—30 versus 70—70, and 50—50 versus 70—70) were performed by twoway repeated measures ANOVA. To examine the effects of ECC2, changes in the criterion measures over time were compared between 30 and 30—30, 50 and 50—50, and 70 and 70—70 groups by two-way repeated measures ANOVA. Comparison between 30—70 and 70—70 groups were also made by twoway repeated measures ANOVA to examine if the 30 eccentric actions performed in the ECC1 had the same effects on ECC2 (70 eccentric actions) as the protocol in which 70 eccentric actions were performed in ECC1. When the ANOVA found a significant interaction (group × time) effect, a Sheff´ e’s post hoc test was conducted to specify the time points where significant differences were evident. Statistical significance was set at P < 0.05. Unless otherwise stated, data are presented as means ± S.D.
Results Blood markers Exercise All subjects visited the laboratory in the morning, and a 10 mL venous blood sample was collected by venipuncture from the cubital fossa region of the dominant arm. The blood was allowed to clot for 30 min at room temperature and centrifuged for 10 min to obtain serum. Serum samples were stored at −20 ◦ C until analysis for CK activity, Mb, and NO concentrations. Serum CK activity was determined spectrophotometrically by a Genstar chemistry analyser (Electro-
All subjects were able to perform the exercise without spotting even for ECC2 that was performed with muscles demonstrated lower MVC compared to the pre-ECC1 level (Fig. 1). However in ECC2, some subjects had difficulty in lowering the dumbbell slowly for extended elbow joint angles (140—170◦ ) and needed to spend a longer time before reaching to the weak angles to keep the eccentric action time for 4—5 s.
Effects of number of eccentric muscle actions on ECC1 and ECC2
61
Figure 1 Changes in MVC (upper two graphs: a and b) and ROM (lower two graphs: c and d) over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a and c) and 30—30, 50—50, 70—70, and 30—70 groups (b and d). Changes in MVC immediately after ECC2 are shown for the groups performed ECC2 (30—30, 30—70, 50—50, and 70—70). Asterisk (*) indicates a significant (P < 0.05) difference between groups. On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
MVC Comparisons among 30, 50, 70 groups, and among 30—30, 50—50, and 70—70 groups, showed that decreases in MVC after ECC1 were significantly smaller (P < 0.05) for 30 eccentric actions compared to 50 and 70 eccentric actions (Fig. 1). MVC recovered to baseline by 10 days after ECC1 for the groups that performed 30 eccentric actions in ECC1, but MVC was not fully recovered at 10 days post-ECC1 for other groups. No significant differences between 50 and 70 groups (P = 0.24), and 50—50 and 70—70 groups (P = 0.26) were evident for the changes in MVC following ECC1. Immediately after ECC2, MVC decreased significantly (P < 0.05) for the 30—30 (5.3%), 30—70 (12.5%), 50—50 (8.2%), and 70—70 (9.1%) groups, and the magnitude of decrease in MVC for the 30—30 was significantly (P < 0.05) smaller than other groups. Despite the decrease in MVC immediately post-
ECC2, MVC recovered to pre-ECC2 level by next day, and no significant differences between 30 and 30—30 (P = 0.31), 50 and 50—50 (P = 0.26), and 70 and 70—70 groups (P = 0.17) were evident. Changes in MVC after ECC2 were not significantly (P = 0.91) different between 30—30 and 30—70 groups.
ROM ROM decreased significantly (P < 0.05) immediately following ECC1, and did not recover for the next 2 days, but started to recover after 3 days postexercise for all groups (Fig. 1). The decreases in ROM after ECC1 were significantly (P < 0.05) smaller for 30 eccentric actions compared to 50 and 70 eccentric actions. No significant differences between 50 and 70 groups (P = 0.78), and 50—50 and 70—70 groups (P = 0.67) were evident
62
T.C. Chen, K. Nosaka
Figure 2 Changes in upper arm circumference over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a) and 30—30, 50—50, 70—70, and 30—70 groups (b). Asterisk (*) indicates a significant (P < 0.05) difference between groups. On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
for the changes in ROM following ECC1. Immediately after ECC2, a significant (P < 0.05) decrease in ROM was evident for the 30—30 (22.6◦ ), 30—70 (26.6◦ ), 50—50 (27.9◦ ), and 70—70 (31.4◦ ) groups, and the magnitude of decrease in ROM for the 30—30 was significantly (P < 0.05) smaller than that of other groups. ROM recovered to pre-ECC2 level by next day after ECC2, and no significant differences between 30 and 30—30 (P = 0.23), 50 and 50—50 (P = 0.10), and 70 and 70—70 groups (P = 0.12) were evident. Changes in ROM after ECC2 were not
significantly (P = 0.56) different between 30—30 and 30—70 groups.
CIR Significant increases in CIR were observed following ECC1 for all groups, and CIR peaked 5—8 days after exercise with 10—13 mm increase from the baseline (Fig. 2). The groups that performed 30 eccentric actions for the first bout (30, 30—30) showed significantly (P < 0.05) smaller increases in CIR fol-
Figure 3 Changes in muscle soreness over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a) and 30—30, 50—50, 70—70, and 30—70 groups (b). On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
Effects of number of eccentric muscle actions on ECC1 and ECC2 lowing ECC1 compared with other groups. No significant differences between 50 and 70 (P = 0.49), and 50—50 and 70—70 (P = 0.30) were seen. No significant (P = 0.93) difference between 30—30 and 30—70 groups was evident for changes in CIR following ECC1.
Muscle soreness Muscle soreness developed significantly (P < 0.05) 1 day after ECC1, peaked 1—3 days, and lasted for 7 days following ECC1 for all groups. No significant differences among the single bout (30, 50, 70) (P = 0.53) and repeated bout (30—30, 50—50, 70—70) groups (P = 0.35) were evident for the changes in muscle soreness following ECC1 (Fig. 3). Changes in muscle soreness were not significantly (P = 0.62) different between 30—30 and 30—70 groups following ECC1.
63
CK, Mb, and NO Serum CK activity and Mb concentration showed significant (P < 0.05) increases at 3 days after ECC1, peaked 4—6 days, and still elevated from the baseline at 10 days after ECC1 for all groups (Fig. 4). Changes in serum CK activity and Mb concentration were not significantly different among the single bout (30, 50, 70) (P = 0.07 for CK and P = 0.21 for Mb) and repeated bout (30—30, 50—50, 70—70) (P = 0.13 for CK and P = 0.34 for Mb) groups following ECC1. Serum NO concentration increased significantly (P < 0.05) 1—4 days after ECC1 for all groups, but no further increases in NO were observed after ECC2 for all groups (Fig. 5). No significant differences between the single bout (30, 50, 70) (P = 0.16) and repeated bout (30—30, 50—50, 70—70) groups (P = 0.11) were observed following ECC1.
Figure 4 Changes in plasma CK activity (upper two graphs: a and b) and myoglobin concentration (lower two graphs: c and d) over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a and c) and 30—30, 50—50, 70—70, and 30—70 groups (b and d). On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
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T.C. Chen, K. Nosaka
Figure 5 Changes in serum NO concentration over 10 days following the first eccentric exercise (ECC1) for 30, 50, and 70 groups (a) and 30—30, 50—50, and 70—70 groups (b). On the top of figures, comparison between 30 vs. 30—30, 50 vs. 50—50, and 70 vs. 70—70 groups are shown. n.s.: no significant difference between groups.
Discussion The originality of the present study was the use of dumbbell for the two bouts of eccentric exercise, and compared among 30, 50, 70 eccentric actions for changes in common markers of muscle damage and NO following single and repeated exercise bouts. The main findings of this study were that: (1) decreases in MVC and ROM, and increases in CIR following ECC1 were significantly smaller for the groups that performed 30 eccentric actions compared to the groups that performed 50 or 70 eccentric actions, and (2) ECC2 performed 3 days after ECC1 did not affect the changes in all criterion measures following ECC1 regardless of the number of eccentric actions. These results confirm the previous studies reporting that a repeated bout of eccentric exercise performed in early recovery days after the initial eccentric exercise does not induce further damage nor retard the recovery6—8 even if more strenuous exercise is performed 3 days after the initial bout.9 One previous study9 used isokinetic eccentric exercise and reported that 70 maximal eccentric actions (70ECC) performed 3 days after 30 maximal eccentric actions (30ECC) did not exacerbate damage nor retard recovery. However, the force generated during 30 or 70 maximal isokinetic eccentric actions in the previous study was approximately 50% lower in the second bout compared to the first bout. This suggests that the second bout was not as strenuous as the first bout in the previous study. In contrast, the present study used the same dumbbell load for the first and second bouts of exercise, and
subjects made maximal effort to perform the second bout similarly to the first bout. Although some subjects had difficulty in lowering the dumbbell slowly for extended elbow joint angles and needed to spend a longer time before reaching to the weak angles, it would appear that the total work of the exercise was similar between bouts, because the weight, movement range, and the time when muscles were activated were the same between bouts. When comparing between the dumbbell exercise in the present study and the isokinetic exercise in the previous study,9 the decreases in MVC and ROM, and the increases in CIR and CK, were greater following the isokinetic exercise than after the dumbbell exercise. This suggests that the dumbbell eccentric exercise was less strenuous than the isokinetic eccentric exercise for the first bout. However, it seems likely that the second bout in the present study was more strenuous than the second bout using the isokinetic exercise in the previous study.9 It is interesting to note that all subjects in the repeated bout group (30—30, 30—70, 50—50, and 70—70) were able to perform ECC2 without spotting, although the MVC immediately prior to ECC2 was significantly lower than that before ECC1 (Fig. 1). It would appear that eccentric force generation is maintained when isometric force (measured 90◦ elbow angle) is reduced. Since the MVC before ECC2 was lower than that before ECC1, it seems that exercise stress induced by ECC2 was larger than that by ECC1, and the dumbbell exercise was more strenuous than the isokinetic exercise for the second bout. However, the findings were not different from those in previous studies.6,9 This suggests
Effects of number of eccentric muscle actions on ECC1 and ECC2 that muscles recovering from the initial damage are not affected by a subsequent exercise bout regardless of the intensity and volume of the exercise bout. Changes in MVC (Fig. 1), ROM (Fig. 1), and CIR (Fig. 2) following ECC1 were significantly smaller following 30 eccentric actions compared to 50 or 70 eccentric actions, and no significant differences between 50 and 70 eccentric actions were found. Moreover, no significant differences among the groups were found for muscle soreness (Fig. 3), serum CK activity (Fig. 4), Mb (Fig. 4), and NO concentrations (Fig. 5). These results suggest that the effect of number of eccentric action was minor, at least among 30, 50, and 70 eccentric actions of the elbow flexors. It may be that muscle fatigue was caused more in the 50 and 70 eccentric actions, and the decrease in ability to produce high force reduced mechanical stress to the muscles. The mechanisms to explain why recovering muscles from eccentric exercise do not suffer from the additional bout of eccentric exercise are unclear. As shown in the present study and previous studies,6—8 it appears that damaged muscle is protected against further damaging stimulus. It has been reported that regeneration of damaged tissue after eccentric exercise takes more than a week.20,21 Considering the short time between ECC1 and ECC2, it seems unlikely that muscle fibres become more resilient in the 3 days after the initial bout. It has been speculated that a population of stress-susceptible fibres is eliminated in the initial bout.1,22 This may explain better the phenomenon of protective effect in a short interval between bouts. It is also reported that optimal angle to generate maximal force shifts to a long muscle length after eccentric exercise18,19 and this is postulated as a mechanism of the repeated bout effect.19 This theory also fits to the short interval repeated bout effect. A recent work9 showed that activation of fast-twitch motor units were reduced in the second bout, and suggested a neural protective mechanism. Further study is necessary to investigate the underlying mechanisms of the repeated bout effect. Serum NO concentration increased significantly by 40% from the baseline 1 and 2 days after ECC1, and elevated for 4 days post-exercise (Fig. 5). To our knowledge, this is the first study to report changes in serum NO concentration after eccentric exercise. It should be noted that the time course of changes in NO were different from that of CK and Mb (Fig. 4), which did not returned to the baseline by 10 days post-exercise. This would suggest that the mechanism of increase in NO is different from that of CK and Mb. Rad´ ak et al.23 reported that NO content
65
in human skeletal muscle increased significantly by 25% at 24 h after 200 eccentric muscle actions of the rectus femoris. The authors suggested that the activation of iNOS in the damaged muscle fibres or activated macrophages in the site of muscle damage was associated with the increase in NO content in the muscle after eccentric exercise.23 It is postulated that increases in blood NO indicate an inflammatory response.15,24 As eccentric exerciseinduced muscle damage also consists of inflammatory responses,2,15,25 the increases in serum NO concentration may reflect inflammation. It has been reported that inflammatory responses last longer than 4 days after eccentric exercise, and usually become more pronounced in the late recovery process in eccentric exercise-induced muscle damage.2,26 However, serum NO concentration showed a largest increase at 1—2 days post-ECC1, and returned to baseline when swelling was most conspicuous (Fig. 2). It would appear that serum NO concentration does not involve in the inflammatory responses after eccentric exercise directly. Further study is necessary to understand the physiological significance of blood NO concentration, and what caused the increase in serum NO after eccentric exercise. In summary, the results of the present study confirmed that repeated eccentric exercise bout performed in early recovery days from initial eccentric exercise did not induce further muscle damage nor retard the recovery process regardless the intensity and volume of eccentric actions performed in the repeated bout. This suggests that muscles recovering from eccentric exercise-induced muscle damage are not affected by additional eccentric exercise; however, the underlying mechanisms are still unknown.
Practical implications • The results of our study confirmed that repeated eccentric exercise bout performed in early recovery days from initial eccentric exercise do not induce further muscle damage nor retard the recovery process regardless of the intensity and volume of eccentric actions in the repeated bout exercise. • They suggest that athletes can perform high volume resistance training at least every 3 days without considering any adverse effects on muscle function and pain sensation. This has confirmed the notion that delayed onset muscle soreness can be ignored, and training with sore muscles does not affect recovery
66 of muscle damage with a minimal chance to suffer from further muscle damage, though it is important to differentiate between eccentric exercise-induced muscle damage and muscle strains/soft tissue injury. • If muscle pain is associated with the injury, an additional bout may be detrimental. Strength coaches and trainers should examine the cause of muscle pain carefully.
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