DISSOCIATED TIME COURSE OF MUSCLE DAMAGE RECOVERY BETWEEN SINGLE- AND MULTI-JOINT EXERCISES IN HIGHLY RESISTANCE-TRAINED MEN SAULO SOARES,1 JOA˜O B. FERREIRA-JUNIOR,1,2 MARIA C. PEREIRA,1 VITOR A. CLETO,1 RAFAEL P. CASTANHEIRA,1 EDUARDO L. CADORE,5 LEE E. BROWN,3 PAULO GENTIL,1 MICHAEL G. BEMBEN,4 AND MARTIM BOTTARO1 1

College of Physical Education, University of Brası´lia, Brası´lia, Brazil; 2Federal Institute of Triangulo Mineiro, Paracatu, Brazil; 3Department of Kinesiology, California State University, Fullerton, California; 4Department of Health and Exercise Science, Neuromuscular Research Laboratory, The University of Oklahoma, Norman, Oklahoma; and 5Department of Physical Education, Federal University of Rio Grande do Sul, Farroupilha, Porto Alegre, Brazil ABSTRACT

Soares, S, Ferreira-Junior, JB, Pereira, MC, Cleto, VA, Castanheira, RP, Cadore, EL, Brown, LE, Gentil, P, Bemben, MG, and Bottaro, M. Dissociated time course of muscle damage recovery between single- and multi-joint exercises in highly resistance-trained men. J Strength Cond Res 29(9): 2594– 2599, 2015—This study compared the time course of elbow flexor muscle recovery after multi- and single-joint exercises in highly resistance-trained men. Sixteen men (24.5 6 5.5 years) performed, in a counterbalanced order, 8 sets of 10 repetition maximum (RM) unilateral seated row exercise and 8 sets of 10RM unilateral biceps preacher curl exercise using the contralateral arm. Maximum isometric peak torque (PT) and delayed onset muscle soreness (DOMS) were recorded at baseline (pre), 10 minutes, 24, 48, 72, and 96 hours after each exercise protocol. There was a significant decrease (p # 0.05) in elbow flexor PT 10 minutes after both the multi- and single-joint exercise sessions. However, PT decrease was greater after single-joint (26.8%) when compared with multijoint (15.1%) exercise (p # 0.05). In addition, elbow flexor PT was lower (8.4%) than baseline 24 hours after the single-joint exercise (p , 0.01), whereas PT returned to baseline 24 hours after the multi-joint exercise. Compared with baseline, DOMS increased at 24, 48, and 72 hours after single-joint exercise (p # 0.05). However, DOMS returned to baseline levels after 72 hours after multi-joint exercise. In addition, DOMS after single-joint exercise was greater (p # 0.05) than after multi-joint exercise at 24, 48, and 72 hours after exercise. Our data suggest that after a resistance training session,

Address correspondence to Saulo Soares, [email protected]. 29(9)/2594–2599 Journal of Strength and Conditioning Research Ó 2015 National Strength and Conditioning Association

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highly resistance-trained men experience dissimilar elbow flexor strength recovery between single-joint and multi-joint exercises. Likewise, elbow flexor DOMS is greater and takes longer to recover after single-joint exercise.

KEY WORDS strength training, exercise choice, elbow flexion, muscle soreness INTRODUCTION

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igh-intensity strength training (ST) promotes an acute decrease in muscle strength that may persist for several hours or days after the training session (5,14,15). This early decrease in muscle strength after ST is associated with neural fatigue and muscle acidosis (1,4,21). However, the reduction of muscle strength for several hours or days (i.e., 8–96 hours) after training is primarily associated with muscle damage (14,15,20). In a study investigating recovery after an ST session, Flores et al. (5) observed that after a training session, composed of eight sets of 10 maximal repetitions (RM), elbow flexor strength fell below baseline levels and remained lower than baseline for 4 days. Similarly, Radaelli et al. (19) observed decreases in elbow flexor muscle strength and increases in delayed onset muscle soreness (DOMS) at 24, 48, and 72 hours after four sets of bicep curls using a 10RM load. Unfortunately, these studies only investigated elbow flexor muscle recovery in untrained subjects (5,19), thus these results may limit the application of subsequent ST sessions in a periodized program in highly resistance-trained subjects. In addition, these studies only assessed elbow flexor muscle recovery after single-joint exercises (i.e., biceps curls); however, the elbow flexors are also recruited during multi-joint exercises such as lat pull-downs and rows (7). Recently, Gentil et al. (7) reported that the stimuli provided by multi-joint exercises (i.e., lat pull-downs) were sufficient to promote muscle strength and size gains in the elbow flexors of untrained subjects after 10 weeks of ST,

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Journal of Strength and Conditioning Research and no additional benefit was achieved when including single-joint exercises (i.e., bicep curls). These results suggest that the mechanical stimuli to the elbow flexors in multi- and single-joint exercises are similar. Moreover, a recent study reported no difference on elbow flexors strength and muscle mass gains between multi-joint (lat pull-down) and single-joint (biceps curls) exercise training (6). They hypothesized that this similar response could be due to similar muscle strain and muscle damage caused by the multi- and single-joint exercises on elbow flexors muscles (6). However, to the best of these authors’ knowledge, no study has investigated the muscle damage and the time course of muscle recovery after multiand single-joint exercises of the elbow flexors in highly resistance-trained subjects. Considering that the performance of strength or power activities could be affected by muscle recovery, further investigation in this area could help strength and conditioning trainers to better set training programs during ST periodization. Thus, the purpose of this study was to compare the time course of muscle strength and DOMS recovery after multi- and single-joint exercises of the elbow flexors in highly resistance-trained men. Our hypothesis was that no differences in strength recovery and DOMS would be observed between exercises.

METHODS Experimental Approach to the Problem

To investigate the time course of muscle recovery after single- and multi-joint strength exercises, sixteen highly resistance-trained men performed two exercise protocols in the same day using a contralateral counterbalanced design: (a) 8 sets of 10RM of unilateral seated row and (b) 8 sets of 10RM unilateral bicep curls using the contralateral arm. Participants attended the laboratory on several different occasions. On the first visit, the experimental procedures were explained. On the second visit, the 10RM loads were assessed. On the third visit, after 72 hours, the 10RM retest was performed, and subjects were familiarized with the peak torque (PT) and DOMS procedures. In subsequent visits, subjects performed the exercise protocols while the maximal PT and DOMS were measured before, 10 minutes, 24, 48, 72, and 96 hours after exercise. To avoid circadian influences, subjects were asked to visit the laboratory always at the same time of day. Volunteers were not allowed to perform any vigorous physical activities or unaccustomed exercise during the experiment period. They were also instructed not to intake medications or supplements during the study period.

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without interruption. Subjects were trained six times a week (split-routine), and they performed an average of 12 sets of 6–12RM for each muscle group twice a week. Volunteers were informed about the design of the study and all possible risks and discomforts related to the procedures. After a verbal explanation of experimental procedures, participants were invited to sign an informed consent form. The study was approved by the Local Institution Ethics Committee and was in accordance with the Helsinki Declaration. Exclusion criteria included any history of neuromuscular, metabolic, hormonal, or cardiovascular diseases. Participants were also excluded if they were taking any medication that could influence hormonal or neuromuscular function. Ten Repetition Maximum Test

To determine the training load to be used during the exercise protocols, 10RMs were assessed in the unilateral biceps curl and unilateral seated row, using a contralateral and counterbalanced design. The 10RM tests were performed on a Scott bench for the biceps curl and on a plate loaded row machine for seated row. Load was adjusted with weight plates starting at 1 kg. On the testing day, subjects warmed up by performing 10 repetitions with 40% of their estimated 10RM (based on their reported training load). Sixty seconds later, they performed 10 repetitions with 60% of their estimated 10RM. Thereafter, each subject’s 10RM load was determined with no more than 5 attempts with a 5minute recovery between attempts. Each repetition took 1 second for the concentric and three seconds for the eccentric action, controlled by an electronic metronome. Test-retest reliability coefficients (intraclass correlation coefficient [ICC]) were 0.93 and 0.83 for the biceps curl and unilateral seated row 10RM values, respectively. Strength Training Protocols

The ST protocols were composed of 8 sets of 10RM unilateral seated row (multi-joint exercise) and 8 sets of 10RM unilateral (contralateral arm) biceps curl (single-joint exercise). Rest intervals were 120 seconds between sets and 10 minutes between exercises. In the second and fifth sets, the load in each exercise was reduced by 10% to avoid a severe reduction in the number of repetitions. The performance time for each repetition was 1 second concentric and three seconds eccentric, controlled by an electronic metronome. The subjects performed both seated row and biceps curl exercise protocols with the hand in a supinated position. Moreover, the range of motion for the elbow joint was controlled for both exercise protocols and ranged from 5–108 (08 full extension) to 120–1308 for both seated row and biceps curl exercises.

Subjects

Sixteen highly resistance-trained men (age: 24.5 6 5.5 years; height: 175.1 6 5.0 cm; mass: 81.8 6 9.1 kg; 10RM unilateral biceps curl load: 17.3 6 4.6 kg; 10RM unilateral seated row load: 47.3 6 8.6 kg) volunteered for the study. Inclusion criteria were ST for at least three years (6.1 6 2.7 years)

Maximal Isometric Peak Torque

To assess the time course of strength changes due to muscle damage, maximal isometric PT was measured by an isokinetic dynamometer (Biodex Medical, Inc., Shirley, NY, USA) immediately before (pre), 10 minutes, 24, 48, 72, and 96 VOLUME 29 | NUMBER 9 | SEPTEMBER 2015 |

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Effect of Exercise Choice on Muscle Recovery session. Researchers provided verbal encouragement during all tests. Maximal PT was defined as the highest value of the torque curve (N$m) recorded during the unilateral elbow flexion repetition. Testretest reliability coefficient (ICC) was 0.96 for the MVIC. Delayed Onset Muscle Soreness

Muscle soreness of the biceps brachii muscle was quantified immediately before (pre), 10 minutes, 24, 48, 72, and 96 hours after the exercise protocols, using the methods Figure 1. Number of repetitions in each set for both multi-joint and single-joint exercise. described by Chen et al. (2). Subjects were asked to describe their muscle soreness level during palpation and stretching on a visual analog scale with hours after the exercise protocols. Subjects were seated with scores ranging from 0 mm (no pain) to 100 mm (extreme their arms placed over the Scott bench positioned close to the pain). Test-retest reliability coefficient (ICC) was 0.86 for dynamometer. Subjects warmed up with 10 elbow extension/ DOMS. flexion repetitions at angular velocity of 908$second21, performing submaximal efforts. All subjects had been familiarized Statistical Analyses with the isometric test protocol 1 week before. Before, 10 miThe Sigma Plot software package was used for all data nutes, 24, 48, 72, and 96 hours after each exercise protocol, analyses. Normal distribution was verified with the Shapirosubjects performed two repetitions of maximum voluntary Wilk test. Results are reported as mean 6 SD. Comparison isometric contraction (MVIC) of the elbow flexors at 908 of between different exercise protocols was performed using flexion (08 full extension) (11). Each MVIC lasted four seca two-way repeated measures analysis of variance (2 protoonds, with 1 minute of recovery between repetitions. The cols 3 6 time points) followed by Tukey’s post hoc analysis. forearm remained in a supinated position throughout the test In addition, reliability of all measurements was calculated by ICC values using single values. The statistical power was greater than 0.85 for all variables, and statistical significance was set at P # 0.05.

RESULTS Strength Training Volume and Peak Torque

Figure 2. Peak torque across all testing sessions for both multi-joint and single-joint exercises. *Lower than pre (p # 0.05); +Difference between multi-joint and single-joint exercise (p # 0.05).

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There was no difference between the multi- and singlejoint exercises based on the number of repetitions performed (p . 0.05) (Figure 1). Peak torque results from baseline, 10 minutes, 24, 48, 72, and 96 hours after the exercise are presented in Figure 2. Before the ST protocols, there was no difference between right and left elbow flexors PT. Following the exercise protocols,

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decreases, along with greater DOMS when compared with multi-joint exercise. In addition, the time course of elbow flexor strength recovery was longer after single-joint exercise compared with multi-joint exercise in highly strengthtrained subjects. Monitoring the relationship among workload, training volume, and the time course of muscle recovery is one of the most important challenges for designing training periodization, especially in high-level sports, competitive weightlifting, and bodybuilding. It is Figure 3. Delayed onset muscle soreness across all testing sessions for both multi-joint and single-joint known that many factors, such exercises. *Greater than pre (p # 0.05). +Difference between multi-joint and single-joint exercise (p # 0.05). as sex differences, age, training status, type of muscle contraction affect the magnitude of there was a significant interaction between protocols and exercise-induced muscle damage (3,17,18). To the best of time points (F = 3.5; power = 0.73; p = 0.01) with a signifithese authors’ knowledge, this was the first study to show cant decrease (p , 0.001) in elbow flexor strength 10 minutes that multi- and single-joint exercise choices may affect the after the exercise session in both single-joint and multi-joint time course of muscle damage recovery. exercises. However, the decrease in strength was greater In this study, the exercise load during multi-joint exercise (p # 0.05) after single-joint (26.8%) when compared with (47.3 6 8.6 kg) was greater than single-joint exercise (17.3 6 multi-joint (15.1% SD). In addition, elbow flexor PT was less 4.6 kg) (p # 0.05). It has been reported that the intensity of (8.4% SD) than baseline at 24 hours after the single-joint resistance exercise can affect muscle damage recovery exercise (p , 0.01), whereas PT returned to baseline levels (14,16,24). Paschalis et al. (16) evaluated the effects of equal at 24 hours after the multi-joint exercise. Moreover, elbow volumes of high-intensity exercise (maximal voluntary conflexor PT at 48, 72, and 96 hours after exercise was similar to tractions) and low-intensity exercise (50% of PT) on muscle baseline after both exercises (Figure 2). damage symptoms. They observed a higher reduction in eccentric and isometric quadriceps PT after high-intensity Delayed Onset Muscle Soreness exercise when compared with low-intensity exercise. Nosaka Before the ST protocols, there was no difference between and Newton (14) found quicker recovery in isometric arms in DOMS (p . 0.05). After the exercise session, there strength, range of motion, muscle swelling, and plasma crewas a significant interaction between protocols and time atine kinase activity after submaximal eccentric exercise points (F = 6.1; power = 0.88; p = 0.003) with a significant (50% of maximal eccentric contraction) compared with maxincrease in DOMS at 24, 48, and 72 hours after single-joint imal eccentric exercise. However, in this study, the higher exercise (p # 0.05), returning to baseline values only after 96 exercise load of the multi-joint exercise did not result in hours. Significant increases in DOMS were also observed at greater muscle damage in the elbow flexors. 24 and 48 hours after multi-joint exercise (p # 0.05), returnA possible reason for the greater muscle damage caused ing to baseline after 72 hours. In addition, DOMS at 24, 48, by the single-joint exercise (biceps curl) compared with the and 72 hours after single-joint exercise was significantly multi-joint exercise (seated row) observed in this study may greater than multi-joint exercise (p # 0.05), whereas no difbe due to the difference in elbow flexor recruitment between ference was observed after 96 hours (Figure 3). each exercise. During back exercises, there is a relative contribution of elbow flexors with a concomitant activity of DISCUSSION shoulder extensors, such as latissimus dorsi, teres major, and pectoralis major (external portion) (12,13,23). However, The aim of this study was to evaluate the muscle damage biceps curl exercise is performed mainly by elbow flexor and the time course of elbow flexor muscle recovery after muscles (9,10). However, the electrical activity assessment multi- and single-joint exercises in highly resistance-trained by electromyography of the elbow flexors during the seated men. The initial hypothesis was not confirmed because the row and biceps curl exercises would have been useful to single-joint exercise induced greater elbow flexor strength VOLUME 29 | NUMBER 9 | SEPTEMBER 2015 |

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Effect of Exercise Choice on Muscle Recovery compare the muscle activity between both exercise protocols. Thus, the lack of these data is a limitation of this study. Moreover, because this is the first controlled study that evaluated the effect of multi- and single-joint exercises on muscle damage recovery, we cannot directly compare our finding with other studies. Gentil et al. (6) reported no difference in elbow flexor strength gains and hypertrophy between multi-joint and single-joint exercise training. Considering that muscle hypertrophy may be dependent on muscle damage and on mechanical and metabolic stresses produced by the strength exercises (22), these authors (6) suggested that muscle damages caused by the multi-joint and single-joint exercises for the elbow flexor muscles were somewhat similar. Nevertheless, the results of this study did not corroborate this hypothesis. It is important to note that we evaluated highly resistance-trained men, whereas the other study evaluated nontrained subjects (6). Strength-trained subjects may present faster muscle recovery, which may be an adaptation to long-term ST (8). Moreover, Gentil et al. (6) did not measure any variable related to exercise-induced muscle damage. In addition, it has been recently shown that the combination of single- and multi-joint exercises does not promote additional elbow flexor muscle hypertrophy when compared with only multi-joint exercises in untrained subjects (7). This finding suggests that the elbow flexors contribution during back exercises (i.e., seated row) and consequently the elbow flexors muscle adaptation to this type of exercise cannot be underestimated. Whether the different elbow flexor muscle recovery observed in this study would result in different muscle adaptations to training in our strength-trained subjects remains to be elucidated. As expected, the exercised-induced muscle damage protocol used in this study caused significant muscle damage, observed through a reduction of 26.7% in PT and an increase in muscle soreness of 45% immediately after and 24 hours after the bicep curl exercise session. This muscle damage corroborates the findings from other studies that investigated elbow flexors muscle recovery after a traditional free weight ST session with multiple sets performed until failure (5,19). Nevertheless, a major limitation of this study was that other indirect markers of muscle damage, such as muscle swelling, muscular enzymes, and inflammatory markers were not measured. In summary, single-joint elbow flexor exercise (biceps curl) induced greater elbow flexor PT decreases and greater DOMS compared with multi-joint elbow flexion exercise (seated row). In addition, the time course of elbow flexor muscle recovery was greater after single-joint exercise compared with multi-joint exercise in highly strengthtrained subjects, even with subjects performing greater workload during the multi-joint exercise compared with single-joint exercise. However, further studies on this topic are necessary to understand the effects that exercise choice has on muscle damage. Additionally, it is important to evaluate the effect of exercise choice on muscle damage

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recovery in other populations, such as athletes, untrained subjects, women, and the elderly.

PRACTICAL APPLICATIONS The results of this study suggest that strength and athletic trainers should take into consideration the effect of multiand single-joint exercises on recovery during ST periodization. Depending on the type of exercise used (i.e., single- and multiple-joints), resistance-trained subjects or athletes might not be able to perform strength or power activities at their best until 24 or 48 hours after the previous exercise bouts.

ACKNOWLEDGMENTS This study was partially supported by the Brazilian Council for the Research Development (CNPq) and by the Brazilian Ministry of Education (CAPES).

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Dissociated Time Course of Muscle Damage Recovery Between Single- and Multi-Joint Exercises in Highly Resistance-Trained Men.

This study compared the time course of elbow flexor muscle recovery after multi- and single-joint exercises in highly resistance-trained men. Sixteen ...
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