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Time Course of Strength and Echo Intensity Recovery After Resistance Exercise in Women

Radaelli, Regis1; Bottaro, Martim2; Wilhelm, Eurico N.1; Wagner, Dale R.3; Pinto, Ronei S.1

Journal of Strength and Conditioning Research: September 2012 - Volume 26 - Issue 9 - p 2577–2584
doi: 10.1519/JSC.0b013e31823dae96
Original Research

Radaelli, R, Bottaro, M, Wilhelm, EN, Wagner, DR, and Pinto, RS. Time course of strength and echo intensity recovery after resistance exercise in women. J Strength Cond Res 26(9): 2577–2584, 2012—The purpose of this study was to evaluate the time course responses of strength, delayed-onset muscle soreness (DOMS), muscle thickness (MT), circumference (CIRC), and ultrasonography echo intensity (EI) after a traditional hypertrophic isoinertial resistance training session in young women. Ten (22.0 ± 3.2 years) healthy, untrained volunteers participated in the study. The resistance exercise session consisted of 4 sets of 10 repetitions at 80% of 1 repetition maximum (1RM) of the dominant arm elbow flexors. Maximum isometric elbow flexion peak torque (PT) at 90°, MT, and EI were recorded for both arms at baseline (PRE), immediately after exercise (0 hours) and at 24, 48, and 72 hours after exercise. Comparisons were made using a 2 × 5 mixed factor analysis of variance. There was a significant (p < 0.05) loss in PT and increase in MT at 0, 24, 48, and 72 hours. In contrast, EI increased only after 24, 48, and 72 hours, not at 0 hours. There were no significant changes in PT, DOMS, MT, and EI in the nondominant (control) arm after the exercise protocol. Our data suggest that after 4 sets of 80% of 1RM of unilateral elbow flexion resistance exercise, nonresistance trained women need >72 hours to fully recover muscle strength, MT, CIRC, and EI. Furthermore, the EI appears to be a sensitive and reliable method to assess MD.

1Exercise Laboratory Research, Physical Education School, Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil

2Strength Training Laboratory, College of Physical Education and Exercise Science, University of Brasília, Brasília, Brazil

3Health, Physical Education, and Recreation Department, Utah State University, Logan, Utah

Address correspondence to Régis Radaelli, regis.radaelli@hotmail.com.

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Introduction

One of the acute variables that determine the adaptations to strength training is the training frequency, and this is related to muscular recovery between training sessions (23,25). Despite the importance of this variable, the optimal amount of time after a resistance training session for adequate recovery has not been well established. Muscular performance recovery between sessions is directly related to different factors, and one of these factors is the muscle damage (MD) induced by the training session (28). Strength training promotes a decrease in force production immediately after the training session mainly because of neural and metabolic factors (3,15,20,35). However, the decrease in strength induced by MD because of high-volume or high-intensity strength training remains longer (13,16). This MD leads to important changes, such as (a) disorganization of sarcomeres occurring mainly in Z lines, (b) damage to the sarcolemma, (c) damage to the T tubules and myofibrils (1,2,19,34), (d) increase in muscle soreness, and (d) increases in levels of blood creatine kinase and potassium (11,22). Associated with these changes, there is an increase in muscle thickness (MT) and in the echo intensity (EI) obtained by ultrasonography (5,15). The EI can be measured from different intensities of the ultrasound image grayscale.

The EI is a relative new and interesting method and has been reported in the literature as an indirect marker of MD. The EI changes related to MD are not usually observed until 24 hours after the exercise session (21,29–31). On the other hand, increases in MT and decreases in force production, which are not because of muscle edema, can be seen immediately after an exercise session. The increase in MT is mainly because of active hyperemia, and the decrease in strength is because of neural and metabolic factors such as a reduction in creatine phosphate concentration and an increase in inorganic phosphate and hydrogen ion concentrations (35,41). Thus, EI may be a better index of MD than the observed changes in MT or strength during the first 24 hours after an exercise session.

Previous studies used the changes in EI to monitor the recovery time of strength training sessions (6,14,19). Nosaka and Newton (28) and Chen et al. (8) observed that even after 96 and 120 hours, respectively, their subjects' EI had not returned to preexercise levels. However, these authors used maximal eccentric contractions and high volumes in their protocols, and during a session of conventional isoinertial strength training, it is more common to perform submaximal eccentric contractions (26). Furthermore, MD is significantly dependent on the intensity of the eccentric phase of each exercise repetition (33). Therefore, these studies may have overestimated the duration of time that EI is elevated after a typical strength training session.

Recently, Flores et al. (14) reported that following 8 sets of 10RM resistance exercise, women and men experienced similar immediate strength loss, but over 4 days, women still had not recovered the strength and MT to baseline level. These authors used high-volume strength training for women, and there is a lack of research on the strength recovery in women using lower volume conventional isoinertial weight training. Furthermore, the EI technique warrants additional investigation, especially when applied to strength training sessions that induce less MD (e.g., submaximal eccentric contractions), before firmly establishing its sensitivity. Thus, the purpose of this study was to evaluate the time course responses of strength, delayed-onset muscle soreness (DOMS), MT, circumference (CIRC), and analyze the EI responses, after 4 sets of traditional hypertrophic isoinertial resistance exercise in young women inexperienced in strength training.

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Methods

Experimental Approach to the Problem

The participants visited the laboratory 6 times. On the first day of the experiment, the subjects performed a baseline elbow flexion 1 repetition maximum (1RM) test. For reliability, the 1RM test was repeated 72 hours later on visit 2. On visit 3, 1 week after the second 1RM test, baseline measures of peak torque (PT), DOMS, MT, and EI were taken from the dominant and nondominant elbow flexors. On the same day (visit 3), the subjects performed a resistance training session consisting of 4 sets of 10 concentric-eccentric repetitions at 80% of 1RM of elbow flexion exercise only with the dominant arm. The dependent variables were assessed at preexercise (PRE), immediately post (0 hours), 24, 48, and 72 hours after the resistance training protocol. All the measures were taken on both arms.

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Subjects

Ten women (22.7 ± 3.2 years) with no resistance training experience and no systematic training in the last year were recruited for the study. The subjects were tested from July to September. Their weight and height were 52.4 ± 3.2 kg and 165.5 ± 5.6 cm, respectively. Before participation, each volunteer read and signed a detailed informed consent form approved by the University Institutional Review Board describing the study and its potential risks and benefits. The subjects were not allowed to perform any vigorous physical activities or unaccustomed exercises during the experiment period. The participants were free from any musculoskeletal disorders and were not taking any medication or dietary supplements.

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Resistance Training Protocol

The resistance training protocol consisted of 4 sets of 10 repetitions of unilateral elbow flexion on a Scott bench (preacher curl, Sculptor, Porto Alegre, Brazil) with a dumbbell resistance equal to 80% of each subject's 1RM and a 3-minute rest interval between sets (25). To determine each subject's concentric after eccentric 1RM, the participants visited the laboratory 2 times. First, the subjects were familiarized with the procedures of the study, and the 1RM load was determined. The subjects returned to the laboratory 72 hours later to repeat their 1RM test. The elbow flexion 1RM load was determined as the heaviest weight the subject was able to lift at either test session, using proper technique with cadence (2 seconds for the concentric phase and 2 seconds for the eccentric phase) controlled by a metronome (Quartz, Torrance, CA, USA). The range of motion of the 1RM test was 10–110° (0° = full elbow extension) and was determined before the test by a goniometer. The range of motion was visually controlled by the researchers. Three minutes of rest was given before each attempt at a higher weight. The 1RM value was determined within 3–5 trials. The baseline test-retest intraclass correlation coefficient (ICC) and SEM for the 1RM were 0.93 and 4.5%, respectively.

One week after the second 1RM test, the subjects returned to the laboratory to perform the resistance training protocol. The elbow flexion exercises were done with only the dominant arm while the nondominant arm served as the control. All the subjects performed the resistance training protocol with the same cadence and range of motion described for the 1RM test (6,30).

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Peak Torque

Unilateral elbow flexion was assessed on a Cybex NORM dynamometer (Ronkonkoma, NY, USA). The equipment was calibrated before the tests according the manufacturer's instructions. The subjects were placed in a supine position with the shoulder of the tested arm abducted 45°, and a velcro strap was across their arm and chest to minimize compensatory movements. Furthermore, the center of rotation of the dynamometer was aligned with the center of rotation of the elbow, and the forearm was supinated. The elbow adapter length was adjusted for each subject, and the participants were instructed to keep their nontested arm at their side. The test consisted of three 5-second maximal isometric voluntary contractions with the elbow flexed at 90° and 3 minutes of recovery between each effort. The greatest PT among 3 isometric voluntary contractions, provided by Humac 2009 software version 12.17.0 (Humac, Stoughton, MA, USA), was used for future analyses.

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Circumference

To measure the arm CIR, the subjects remained supine with their arms relaxed at their sides. The CIR was measured with a tape measure, 8 cm above the elbow joint (9). The CIR measurement site was marked with a dermographic pen and remained visible till the end of the study.

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Delayed-Onset Muscle Soreness

Muscle soreness was quantified using the methodology described by Chen et al. (7,9). The subjects were asked to indicate their level of muscle soreness on a 100-mm visual analog scale (0 mm “no pain” and 100 mm “extreme pain”) after full range of flexion and extension at the elbow. The specific location being assessed for DOMS was the mark 8 cm above the elbow joint described previously.

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Muscle Thickness and Echo Intensity

The MT and EI were assessed by ultrasonography according to the same methodology used by other authors (5,6,28). The images were obtained by B-mode ultrasonography (Ultravision Flip plus, Philips, Belo Horizonte, Brazil). Both images (MT and EI) were obtained at 8 cm above the elbow joint (8). During the image acquisition, the subjects remained supine with the tested arm relaxed. The high resolution with a linear probe of 7.5 MHz was positioned perpendicular to the evaluated muscles. A water-based gel was used to promote acoustic contact without causing excessive probe pressure on the skin during imaging acquisition. In each image, both biceps brachii and brachialis MT were identified. The coefficient of variation was 4.2%, and the baseline test-retest ICC was 0.94. The same image used to assess MT was used to measure the EI. The EI in each of the elbow flexor muscles was determined using a 1-cm2 region, based on a histogram of gray scale (0: black, 256: white). The EI was quantified using the Image-J software (version1.37, National Institutes of Health, Washington, D.C., USA). The test-retest reliability presented ICC for EI was 0.91, and the coefficient of variation was 2.2%.

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Statistical Analyses

All the values are reported as mean ± SD. Normality of the distribution for outcome measures was tested using the Kolmogorov-Smirnov test. After assuming that the sample was normally distributed (p > 0.05), comparisons were made using a 2 × 5 (arm [dominant and nondominant] × time [Pre, 0, 24, 48, 72 hours]) mixed factor analysis of variance (ANOVA). When the ANOVA showed a significant main effect, Bonferroni post hoc tests were used to detect differences in the value between bouts. A 2 ×5 (muscle [biceps brachii and brachialis] × time [Pre, 0, 24, 48, 72 hours]) was used to analyze MT and EI differences between muscles. Dependent variables were PT, DOMS, CIR, MT, and EI. The ICC for the 1RM test-retest reliability was also performed. Significance was set at p < 0.05. All analyses were performed with the software SPSS 17.0 (IBM, Somers, NY, USA).

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Results

Peak Torque

The PT was significantly lower in the dominant arm at all time points postresistance exercise when compared with that in the nondominant arm (Figure 1). In the dominant arm, PT significantly (p < 0.05) decreased between 12 and 16% after the resistance training protocol (0 hours = 16%; 24 hours = 12%; 48 hours = 14%; 72 hours = 15%). There were no significant (p > 0.05) differences across time in PT for the nondominant arm.

Figure 1

Figure 1

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Circumference

The CIR was significantly higher in the dominant arm at all time points postresistance exercise when compared with that in the nondominant arm (Figure 2). In the dominant arm, CIR significantly (p < 0.05) increased between 2 and 3% (0 and 24 hours = 2%; 48 and 72 hours = 3%) after the resistance training protocol. There were no significant (p > 0.05) differences across time in CIR for the nondominant arm.

Figure 2

Figure 2

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Muscle Soreness

The DOMS was significantly higher in the dominant arm at 24 and 48 hours when compared with that in the nondominant arm (Figure 3). In the dominant arm, DOMS significantly (p < 0.05) increased between 31 and 49% (0 hours = 0%; 24 hours = 49%; 48 hours = 31%; 72 hours = 0%) after the resistance training protocol. There were no significant (p > 0.05) differences across time in DOMS for the nondominant arm.

Figure 3

Figure 3

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Muscle Thickness

The biceps brachii MT was significantly higher in the dominant arm from 0 to 72 hours when compared with that in the nondominant arm (Figure 4A). In the dominant arm, biceps brachii MT significantly (p < 0.05) increased between 3.6 and 9.9% (0 hours = 9.9%; 24 hours = 5.6%; 48 hours = 5.4%; 72 hours = 3.6%) after the resistance training protocol. There were no significant (p > 0.05) differences across time in biceps brachii MT for the nondominant arm.

Figure 4

Figure 4

At 0 to 72 hours, the brachialis MT in the dominant arm was significantly higher (p < 0.05) than that in the nondominant arm (Figure 4B). The increase in the dominant brachialis MT was between 2.9 and 9.7% (0 hours = 9.7%; 24 hours = 5.6%; 48 hours = 3.8%; 72 hours = 2.9%). There were no significant (p > 0.05) differences across time in brachialis MT for the nondominant arm. Also, there were no significant differences (p > 0.05) in the MT between biceps brachii and brachialis after the resistance training protocol.

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Echo Intensity

The EI was assessed from both elbow flexor muscles (biceps brachii and brachialis). The biceps brachii EI was significantly higher in the dominant arm at 24, 48, and 72 hours when compared with that in the nondominant arm (Figure 5A). In the dominant arm, EI significantly (p < 0.05) increased between 6 and 14% (0 hours = 0%; 24 hours = 6%; 48 hours = 11%; 72 hours = 14%) after the resistance training protocol. There were no significant (p > 0.05) differences across time in EI for the nondominant arm.

Figure 5

Figure 5

At 24, 48, and 72 hours, the brachialis EI was significantly higher in the dominant arm when compared with that in the nondominant arm (Figure 5B). In the dominant arm, EI significantly (p < 0.05) increased between 2 and 5% (0 hours = 0%; 24 hours = 2%; 48 hours = 4%; 72 hours = 5%) after the resistance training protocol. There were no significant (p > 0.05) differences across time in EI for the nondominant arm. However, a significant difference (p < 0.05) in EI was observed at 24, 48, and 72 hours between biceps brachii and brachialis.

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Discussion

The main finding of this study was that the recovery period of 72 hours was not enough time to promote the recovery of muscle strength, CIR, MT, and EI induced by a protocol of 4 sets of 10 repetitions of elbow flexion at 80% of 1RM in untrained young women. Also, an important finding was that, unlike the other dependent variables (PT, CIR, and MT), the EI from the biceps brachii and brachialis did not change immediately after the exercise protocol. These findings showed that EI is a useful tool to indirectly assess MD.

The major consequence of MD is the prolonged reduction in strength production capacity, and this is one of the most reproducible indicators of MD (1,3). The decrease in strength production observed immediately after exercise is not because of MD but to peripheral (within the muscle) and central (reduced motor drive) neuromuscular fatigue (13). For example, Raastad and Hallén (33) observed a decline of 22% in electrically evoked force after 50-Hz stimulation, after high- and moderate-intensity strength exercises of the knee extensors, indicating that the reduction in performance was of peripheral origin; however, the authors did not exclude a central fatigue theory. The reduction in creatine phosphate concentration and increases in inorganic phosphate and hydrogen ion concentrations (35,41) are also possible causes of force reduction immediately after exercise. However, the prolonged decline in the capacity to produce strength seems to be a consequence of MD and an impaired excitation-contraction relationship, in which less Ca2+ is released from the sarcoplasmic reticulum by the action potential (21,32,33). Ingalls et al. (21) noted that an impaired excitation-contraction relationship was the primary mechanism associated with prolonged force loss. The 15% reduction in the ability to produce strength 72 hours after the exercise protocol observed in our study was lower than that reported by others (14,27,28,31), probably because of the differences in the volume and intensity between the exercise protocols. Because MD is associated with eccentric intensity, the lower intensity of eccentric contractions and exercise volume of this study compared with the others better mimic traditional strength training programs.

The recovery in force production in our results was lower than in other studies (12,18). Also, this study and others (17,24) suggest that muscle strength does not recover after 72 hours. Häkkinen et al. (18) showed that women of various ages unaccustomed to resistance training experienced an 18.8–30.9% decrease in strength immediately after a lower-body workout consisting of 5 sets of 10 repetitions with a 10RM load. They recovered only 94% of their strength 2 days after the workout. Similarly, Logan and Abernethy (24) observed that 3 days of rest is required to recover strength in experienced lifters. Therefore, the recovery in strength, among our and other studies, may be dependent on the intensity of eccentric contractions, volume, and muscle groups involved.

Other studies found decreases in force production and increases in EI (7,29); however, the relationship between them was not discussed previously in the literature. The highest increase in EI generally is observed 3–4 days after exercise (27,29). This study observed the highest value of biceps brachii and brachialis EI at 72 hours postresistance exercise. Thus, the increase of EI, which is related to edema formation (15), might be more predictive of prolonged (e.g., 72 hours postworkout) rather than immediate performance decrement, because at 0-hour, muscle fatigue is primarily responsible for strength loss (35,41).

The increase in CIR, and MT, reinforced that a period of 72 hours was insufficient for the complete MD recovery from the exercise bout. The increases in CIR and MT are the result of MD, the inflammatory process, and protein synthesis (9,37). Thus, for young women untrained in strength, 72 hours was not a sufficient amount of time to observe a full recovery from inflammation induced by the exercise protocol. Muscle soreness is also widely used as an indirect indicator of MD (7,10). The soreness peak is generally observed 24–48 hours after exercise (10) as seen in our results. Also, Nosaka and Clarkson (27) observed that DOMS was developed 1 to 3 days after exercise, whereas CIR was largest at 4–5 days after exercise. One cause of this phenomenon might be that the stimuli for the sensation of muscle soreness may be the pressure inside the muscle, but swelling itself does not necessarily cause soreness (4,20). The significant reduction in DOMS 72 hours postexercise in our study, despite the other indirect markers of MD remaining elevated, supports other research studies suggesting that muscle soreness does not reflect the magnitude of the MD induced by exercise (30,40). However, at 24 and 48 hours postexercise DOMS peaked and force production was at its lowest; thus, these data suggest that DOMS may be a good indirect marker between 24 and 48 hours after exercise.

An increase in EI values has been used as an indicator of MD after an exercise bout (15,27,31). However, to our knowledge, this is the first study to use the EI to analyze the MD induced by a traditional isoinertial resistance training session. The results showed that the EI was a sensitivity method to measure MD induced by resistance training. The increase in EI may be associated with an increase in the interstitial space between fibers, which results from muscle swelling or increase in plasma enzyme levels (15). Although it was not the main objective of the study, it is important to note that the increase in the EI of the biceps brachii muscle was greater than the brachialis at 24, 48, and 72 hours (Figures 5A and B). However, there were no differences in MT between biceps brachii and brachialis across time after the exercise protocol. It is important to observe that MT increased 14% in biceps brachii and only 5% in brachialis. However, the EI difference between biceps brachii and brachialis was only 0.2% (9.9 vs. 9.7%). These findings draw attention to the sensitivity of the EI measurement. Furthermore, the differences between these 2 muscles in muscle architecture and activation may have caused this difference in the magnitude of EI increases. Allen et al. (2) observed that the biceps brachii has a greater activation in relation to the brachialis during elbow flexion, a fact that may have contributed to this difference in this indirect marker of MD. However, further studies are needed to better clarify these differences in MD between the biceps brachii and brachialis muscles after bouts of elbow flexion. Also, an important finding from this study is that EI at 0 hours does not change, and MT and CIR significantly changed at 0 hours. The increase in MT and CIR at 0 hours is mainly related to the active hyperemia and not to the MD. Active hyperemia is the increase in organ blood flow (hyperemia) that is associated with increased metabolic activity of a muscle contraction. However, the increase in EI is not related to hyperemia, rather it is likely associated with inflammatory responses. Fujikake et al. (15) noted that the increase in EI was not caused by infiltration of inflammatory cells; however, in this same study, the authors demonstrated that the inflammation responses such as edema might be associated with increases in the EI at 24 and 48 hours. The increase at 72 hours after the exercise might be associated with the production of new connective tissue (27). Thus, these results showed that EI may be a better index of MD than MT or CIR because active hyperemia does not influence the EI measurements (36).

Regarding the period of recovery between exercise bouts, the results of our study confirm the information that sessions that include eccentric contractions may require a period of at least 72 hours for muscle recovery (23). The fact that impairments in neuromuscular function were still observed 72 hours after a protocol of conventional strength training may have important implications in the next session of training. Because of the temporary decrease in the ability to produce strength, the subject may not be able to accomplish the total volume estimated for the session, and this variable has an important influence on neuromuscular adaptations (23,39,40). In a longitudinal study, Häkkinen et al. (18) found that women who underwent training sessions 3 times a week showed smaller increases in muscle strength than those subjected to it twice per week. These authors explained that the results were obtained possibly because of incomplete muscle recovery between training sessions in the high-frequency group. Thus, based on the findings of Häkkinen et al. (18) and the results of this study, women unaccustomed to resistance training should wait at least 72 hours before starting the next training session for the same muscle group.

A limitation of this study is that we did not control for the subjects' menstrual cycle. The literature suggests that estrogen has a protective function in the muscle cell membrane to the damage induced by exercise (38). Thus, different stages in the menstrual cycle may have influenced the magnitude of damage and recovery.

In conclusion, 72 hours of recovery after a protocol of conventional strength training was not sufficient to promote a complete recovery of elbow flexor muscles of young women unaccustomed to strength training. The results highlight the need for adequate control of the recovery period between sessions, especially during initial training. Also, we found that EI, assessed by ultrasonography, is a sensitivity and reliable measurement of MD induced by a traditional resistance exercise protocol.

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Practical Applications

The recovery time between resistance training sessions is one important variable that should be controlled in periodized training programs, and a well-planned training program should consider complete muscular recovery before beginning the next training session for the same muscle group. Therefore, according to our results, the exercise technicians or strength coaches should wait at least 3 days before starting the next training session of the same muscle group during the first weeks of training to ensure adequate recovery in novice lifters. Furthermore, because portable ultrasound is gaining popularity and becoming more accessible, and the EI measurement technique is relatively easy, EI assessments can help strength and conditioning coaches to better monitor recovery among training sessions.

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Acknowledgments

The authors thank the anonymous reviewers for their insightful comments in the formulation of this article.

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Keywords:

resistance exercise; muscle damage; muscle thickness

© 2012 National Strength and Conditioning Association