Objectives: Large inter-subject variability in responses to eccentric exercise has been reported. This study investigated the hypothesis that the variability of changes in indirect markers of exercise-induced muscle damage (EIMD) would be explained by work performed and/or torque generated during eccentric exercise.
Methods: Subjects (n = 53) performed 60 maximal eccentric actions of the elbow flexors on an isokinetic dynamometer that forcibly extended the elbow joint from 60° to 180° at a constant velocity (90° s−1). Markers of EIMD included maximal voluntary isometric contraction torque at 90° elbow flexion (MVC), range of motion, plasma creatine kinase activity and muscle soreness. Measurements were taken 2 days before, immediately after and 1–4 days post-exercise. Pearson’s correlation coefficient was used to examine relationships between exercise parameters (total work, change in total work, torque produced during exercise, change in peak torque) and markers of EIMD.
Results: Large inter-subject variability was evident for both work and torque during exercise, and changes in all markers of EIMD. Contrary to the hypothesis, total work (normalised for individual pre-exercise MVC) did not correlate significantly with any markers of EIMD, with the exception of MVC (r = 0.3). Total work performed and changes in total work showed higher correlations with some markers, but no r-values exceeded 0.4. Normalised exercise torque and the changes in peak torque during exercise were not correlated with changes in MVC, or other markers.
Conclusion: These results suggest the large inter-subject variability in responses to eccentric exercise is not associated with work performed or torque generated during eccentric exercise.
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It is well known that novel and/or unaccustomed exercise consisting of lengthening muscle contractions (eccentric exercise) results in muscle damage.1 2 Muscle damage can be assessed via measures of isometric or dynamic strength, range of motion (ROM) about a joint, blood levels of muscle-specific proteins and muscle soreness.3–5 It has been shown that changes in these markers are influenced by a variety of factors, including exercise intensity,6 7 number of muscle contractions during exercise,8–10 exercised muscle length10 11 and exercise performed prior to eccentric exercise.12 13 However, even when such factors are controlled, a large inter-subject variability in the changes in the markers after exercise still exists.14
Animal studies have shown that critical factors determining the magnitude of muscle damage include torque generated, work performed and strain imposed during eccentric exercise.10 15 16 Lieber and Fridén,16 and Brooks and Faulkner17 have demonstrated that the strain, defined as the rate of deformation beyond optimum, is a primary factor for eccentric exercise-induced muscle damage. Another study showed that work done during a single stretch of maximally activated in situ mouse extensor digitorum longus (EDL) muscle best predicted the magnitude of force decrement.18 Warren et al15 using an isolated rat soleus muscle model, demonstrated that changes in muscle function correlated strongly with peak forces generated during lengthening contractions. However, no previous human studies have investigated the relationship between forces produced or work performed during voluntary eccentric exercise and changes in muscle function, muscle soreness and other common markers of muscle damage.
It may be that the large variability in the changes in common markers of muscle damage after eccentric exercise can be explained by the variability in force and/or work produced in the exercise. It was hypothesised that the higher torques generated and the greater work performed during eccentric exercise (relative to pre-exercise maximal voluntary strength), the greater the changes in muscle damage markers. To investigate this proposition, we collated previously unreported results from several studies in our laboratory on subjects from the same population who underwent a standardised exercise protocol, and analysed the relationship between work performed and torque generated during eccentric exercise and changes in muscle strength, ROM, plasma creatine kinase (CK) activity and muscle soreness.
Subjects were 53 healthy men (mean (SD) age 27.2 (5.9) years, height 1.7 (0.1) m, weight 77.4 (14.3) kg) recruited from the student population of Edith Cowan University. Subjects were physically active but had not been involved in resistance training for at least 6 months prior to participating in this study. All gave written informed consent prior to participation. Approval for the study was granted from the institutional Human Research Ethics Committee, which met the standards set by the declaration of Helsinki on medical research using human subjects. Subjects were requested not to take any medication and nutritional supplements, change their diet or perform any strenuous exercise during the experimental period.
The exercise protocol consisted of 60 maximal voluntary eccentric contractions of the elbow flexors at a constant angular velocity (90° s−1), performed in 10 sets of six maximal eccentric contractions, with a 3 min rest period between sets. Exercise and strength testing were conducted using an isokinetic dynamometer (Cybex 6000, Ronkonkoma, NY, USA), with data recorded using a PC interface operating AMLAB data acquisition software (version II, Lewisham, Australia). Torque and lever arm position data were accessed from the dynamometer and sampled via a 16-bit data acquisition card (Minirack, AMLAB II, Lewisham, Australia). The ROM used was 120° starting at an elbow flexion of 60° and lengthening to full extension (180°). Subjects were positioned individually on the isokinetic dynamometer with their arm supported at 45° of shoulder flexion on an arm preacher curl bench. Subjects were verbally encouraged throughout each eccentric action of the elbow flexors to apply maximal resistance against the lever arm, and were provided with visual feedback to maximise torque output for each contraction.
Work and torque during exercise
Total work performed during the exercise (Total Wk) was calculated using custom programming functions in the AMLAB acquisition software. Total Wk was normalised to pre-exercise maximal voluntary isometric contraction or maximal voluntary isometric contraction strength (MVC) (Wk/MVC) in the assumption that the ratio would provide a better indication of exercise performance, since the absolute work value is dependent on MVC. The work of each eccentric contraction was calculated, and per cent change in the work from the first contraction to the 60th contraction was obtained for each subject. Maximum work generally occurred in the first set, and the minimum work in the last set, with the maximum change in work (%Δ Wk) obtained using the following formula:
%Δ Wk = ((maximum work of a contraction − minimum work of a contraction)/maximum work of a contraction) × 100
The peak torque (Pt) generated in each of 60 eccentric contractions was obtained, and maximum per cent change in torque (%Δ Pt) for each subject was calculated by the following formula (in most cases, the maximum torque was found in the first set, and the minimum torque was in the last set):
%Δ Pt = ((maximum torque of a contraction − minimum torque of a contraction)/maximum torque of a contraction) × 100
Similar to the Wk, the Pt was normalised to each subject’s maximal pre-exercise MVC (Pt/MVC). The torque generated during eccentric contractions, especially before muscle fatigue occurred, was expected to be higher than that during isometric contractions.
Markers of muscle damage
The markers of muscle damage included MVC at 90° of elbow flexion, ROM, CK activity and muscle soreness, which were commonly used as indirect markers of muscle damage in previous studies.5 6 19 All markers were measured 2 days before (pre-exercise) and 1–4 days post-exercise; MVC and ROM were also measured immediately and 1 h post-exercise. The test−retest reliability as indicated by the coefficient of variation (CV) for MVC, ROM, CK and muscle soreness was 4.9%, 1.0%, 4.1% and 0%, respectively.
Maximal voluntary isometric contraction strength (MVC)
The body positioning of subjects for the MVC measures was the same as that described in the eccentric exercise section. MVC was measured at the elbow joint angle of 90° where full extension was considered as 180°. The elbow joint angle (90°) was determined in the pre-exercise measurement, and the same joint angle was used throughout the time period of the investigation, regardless of changes in range of motion by the exercise. The peak torque of two 4 s contractions was measured with a 60 s rest between contractions, and the mean of the two peak torque values was used for further analysis.
Range of motion (ROM)
Elbow joint angles were measured by a goniometer with the subject in a standing position while maximally flexing (Flx) or maximally extending (Ext) the elbow joint angle. The difference between the two angles (Flx and Ext) was defined as ROM.
Plasma creatine kinase activity
Plasma CK activity was determined from a 30 μl sample of whole blood collected from a fingertip puncture made using a spring-loaded lancet. The sample was collected into a heparinised capillary tube and immediately pipetted onto a test strip for analysis using a Reflotron spectrophotometer (Boehringer-Mannheim, Pode, Czech Republic). For this technique, normal values are in the range 20–220 IU/l.
Muscle soreness (SOR)
Muscle soreness was assessed using a 100 mm visual analog scale where the subject was instructed that 0 mm indicated no pain at all while 100 mm was an indication of “unbearable” pain. Subjects were asked to rate the soreness experienced during each measure by making a mark on the 100 mm line. Subjects were asked to keep their arm relaxed while the elbow joint was forcibly flexed and extended for the full ROM by the investigator, providing a rating of soreness for both flexion and extension. Soreness resulting from palpation of the upper arm and forearm was also assessed whilst the arm was palpated in four marked positions (3–5 cm and 9–11 cm above the elbow crease, brachialis and brachioradialis). The same investigator performed all soreness assessments throughout the experimental period, and the procedure for flexion/extension and palpation pressure was kept as constant as possible between days and between subjects. An average of the six measures was used for further analysis.
Analysis was conducted using the software package SPSS (version 12) with a statistical significance set at p<0.05. Markers of muscle damage were analysed using a one-way repeated measures ANOVA (measure × time). Pearson’s correlation coefficient was used to analyse correlations between the variables of work or torque during exercise and the markers of muscle damage at each time point (post, 1–4 days post-exercise). MVC and ROM were normalised to baseline, and the normalised values were used for the correlation analyses; however, absolute values were used for CK and SOR. The results are presented as mean (SEM) unless otherwise stated.
Work and torque during exercise
Total work performed over 60 eccentric contractions ranged between 695 and 7702 J. Figure 1A shows changes in average work performed for each set over 10 sets. Average work for the first set (441 (27) J, range 96–858 J) declined significantly by the 3rd set (411 (26) J) and continued to decline by the 10th set (305 (20) J; range 67–653 J). The average %Δ Wk showed a large variability among subjects (fig 1B) ranging between 25% and 92% of the first set. Average eccentric peak torque ranged from 18.7−92.5 Nm for set 1 to 13.5–65.8 Nm for the 10th set, decreasing significantly (fig 1C). The %Δ Pt also showed a large inter-subject variation (fig 1D) with declines of 25–91% of baseline.
Relationships between the pre-exercise MVC and work or torque are shown in fig 2. The pre-exercise MVC and total work (fig 2A) were highly correlated. A high correlation was found between the pre-exercise MVC and average torque generated in the first set (fig 2B), and this was also the case for other sets. A significant negative correlation between pre-exercise MVC and %Δ Wk (fig 2C) was observed, while no significant relationship was evident between pre-exercise MVC and %Δ Pt (fig 2D).
Figure 3 shows a categorisation of subjects for total work and torque produced during exercise in relation to their pre-exercise MVC. When total work performed was normalised to each subject’s pre-exercise MVC, a large variability was evident (fig 3A). Mean eccentric torque of the first set (six contractions) varied among subjects with a range of 18–92 Nm; however, the greatest average torque was always recorded in this set for all subjects. When peak torque during eccentric exercise was normalised for each subject’s pre-exercise MVC, the ratio was less than 1 for most subjects (mean 0.94 (0.02)), ranging between 0.65 and 1.49 (fig 3B), indicating most subjects were unable to develop greater eccentric torque than their pre-exercise MVC even during the first set. In the following sets, because of the decrease in eccentric torque (fig 1C), the ratio became lower than that of the first set.
Markers of muscle damage
Baseline MVC ranged between 16.4 and 108.4 Nm with the average of 62.9 (2.6) Nm. Decreases in MVC were greatest (59.2 (1.5)% of pre-exercise) immediately post-exercise, with marginal recovery 1 day post-exercise (60.4 (1.6)%), and MVC remained significantly lower than the baseline (73.6 (2.4)%) at 4 days post-exercise (fig 4A). Prior to exercise, subjects’ mean ROM was 132.2 (1.1)°, varying between 108.5° and 155.8°. The greatest reduction in ROM was observed 3 days post-exercise with 120.4 (1.7)° ranging between 85° and 144° (fig 4B). No muscle soreness was reported in any subject prior to exercise, but 1 day following exercise the average perceived soreness score ranged between 0 and 70 mm (21.6 (2.1) mm), peaked 2 days post-exercise (29.1 (2.0) mm) and remained elevated 4 days post-exercise (17.7 (2.0) mm) (fig 4C). Prior to exercise, subjects exhibited a large variation for plasma CK activity ranging from 36 to 502 IU/l (139.3 (11.4) IU/l). The peak in plasma CK activity following exercise occurred 4 days post-exercise (1780.1 (388.3) IU/l); however, subject responses differed greatly, varying from 106 to 17700 IU/l (fig 4D).
Relationships between exercise parameters and indicators of muscle damage
All variables were compared across each time point and peak; however, only correlations for maximum change (Max), day 1 (D1) and day 4 (D4) are shown in table 1, since these values represented the values of other time points. None of the investigated exercise parameters—total work (Total Wk), total work normalised by pre-exercise MVC (Wk/MVC), change in work (%Δ Wk), change in exercise peak torque (%Δ Pt) and exercise peak torque normalised by pre-exercise MVC (Pt/MVC)—correlated highly with any markers of muscle damage.
To the best of our knowledge, this is the first study to investigate the relationship between work and torque during eccentric exercise, and the magnitude of changes in common markers of muscle damage in humans. Correlations between the exercise parameters and muscle strength, ROM, CK and muscle soreness were low or absent (table 1). Thus, the findings of the present study do not support the hypothesis that differences in the magnitude of changes in the markers of muscle damage after eccentric exercise among subjects can be explained by the changes in work performed or torque generated during exercise.
It has been reported that forces developed during active stretch of an animal muscle correlate with the extent of the resultant decrease in muscle strength.10 15 Figure 1A and 1C clearly demonstrate that a large variability exists for the level of eccentric torque generated during 60 eccentric contractions among subjects. Although all subjects were putatively activating their elbow flexors maximally during each contraction, the percentage change between subjects was highly variable (fig 1B,D). It should be noted that “maximal voluntary” contractions were not verified if they were indeed “maximal;” however, it seems reasonable to assume that all subjects performed the exercise as instructed, and they provided maximal efforts. As shown in fig 2A,B, work performed and torque generated during eccentric exercise are dependent on pre-exercise MVC; the greater the MVC, the more work performed and torque generated. However, the %Δ Wk performed and %Δ Pt generated during exercise did not have a strong relationship with the pre-exercise MVC (fig 2C,D). This suggests that the pre-exercise MVC does not strongly predict change in work and torque over 60 eccentric contractions. This lack of a strong relationship for %Δ Pt may be indicative of the peak torque measurement being position specific, whereas %Δ Wk is representative of the whole range of movement, and the latter may be more sensitive to changes in contractile function. The strong relationship between pre-MVC and total work performed or average eccentric torque of the 1st set indicates that when a subject’s pre-strength level is accounted for the ratios provide an indication as to how well a subject maintained force production during the exercise.
Following normalisation of work and torque by pre-exercise MVC, a large variability was still evident (fig 3A,B). Previously we reported that eccentric strength is 15–20% greater than isometric strength for the elbow flexors.20 It is evident from fig 3A that some subjects were able to generate higher force during an eccentric contraction than an isometric contraction, but the majority of subjects were unable to generate greater peak eccentric torque compared to isometric MVC (fig 3B). It is unknown why force generated during eccentric exercise at least for the first several contractions was not necessarily greater than isometric MVC. However, considering the fact that the ratio between pre-exercise MVC and torque during eccentric exercise did not predict the magnitude of changes in markers of muscle damage (table 1), it would appear that high force is not the primary factor to determine the magnitude of muscle damage following voluntary eccentric contraction.21 It has been reported that muscle torque generated at a longer exercised muscle length is associated with the magnitude of muscle damage22 and that the loss of voluntary activation is length specific for the elbow flexors, with a greater loss of voluntary drive at shorter muscle lengths.23 It is possible to assume that force production at long muscle lengths relative to the MVC varied among subjects, and subjects who generated relatively greater force at longer muscle lengths had greater changes in markers of muscle damage. Further study is necessary to investigate the relationship between the force generation level at long muscle lengths relative to pre-exercise MVC and changes in MVC after exercise.
The changes in muscle function and soreness after exercise in the present study were similar to those reported previously8 24 (fig 4A−D). The performance of 60 eccentric actions of the elbow flexors at 90° s−1 resulted in significant decrements in isometric strength and ROM, elevated levels of palpated muscle soreness and significant increases in plasma CK activity 4 days post-exercise (fig 4A−D). The extent of subject variability recorded following isokinetic exercise is similar to the variability previously described following manually controlled eccentric exercise.14 Measures of work performed during exercise (Total work, Wk/MVC and %Δ Wk) demonstrated a significant correlation with many of the variables including ROM and SOR; however, the correlations were not strong (table 1).
The reasons for the variability in responses to EIMD have yet to be fully elucidated and require further investigation, since the results of the present study did not support the hypothesis that the variability of changes in indirect markers of muscle damage would be explained by work performed and/or torque generated during eccentric exercise. It has been documented recently that the variability in responses to eccentric exercise among subjects can be explained by genetic differences such as the genes coding for α-actinin 3 and myosin light chain kinase (MLCK),25 or IGF-II.26 Clarkson et al25 reported that specific single nucleotide polymorphisms (SNPs) in MLCK were associated with the magnitude of changes in CK activity and myoglobin (Mb) concentration in the blood, and maximal voluntary isometric strength. Devaney et al26 have recently reported that IGF-II gene region polymorphisms are related to strength loss, muscle soreness, and CK and Mb responses to eccentric exercise of the elbow flexors in men but not in women. They suggest that SNPs in some genes may explain the inter-subject variability in responses to eccentric exercise; however, it seems unlikely that the genotype alone can explain the variability. It is speculated that individual differences in fibre type composition and muscle architecture would also account for some of the variability.27 28 It is possible to assume that subjects who are less susceptible to EIMD have a greater percentage of slow twitch fibres, and/or have muscle fibres with a greater number of sarcomeres in series. Lifestyle factors such as working environment and daily lifting activities would also impact on the response to maximal eccentric exercise. Further study is necessary to elucidate the factors responsible for the large inter-subject variability in responses to eccentric exercise.
What is already known on this topic
Unaccustomed eccentric exercise leads to a prolonged impairment of muscle function and delayed onset muscle soreness.
A large inter-subject variability exists for the responses of indirect markers of muscle damage.
What this study adds
A large inter-subject variability exists for the torque produced and/or work performed during eccentric exercise.
Neither of the exercise parameters can explain the large variability in changes in muscle strength, range of motion, plasma CK activity and muscle soreness after eccentric exercise of the elbow flexors.
Competing interests: None declared.