Acta Physiologica Hungarica, Volume 101 (2), pp. 150–157 (2014) DOI: 10.1556/APhysiol.101.2014.2.3

Muscle damage after low-intensity eccentric contractions with blood flow restriction RS Thiebaud1, JP Loenneke1, CA Fahs1, D Kim1, X Ye1, T Abe2, K Nosaka3, MG Bemben1 1

University of Oklahoma, Norman, OK, USA, 2 Indiana University, Bloomington, IN, USA 3 Edith Cowan University, Joondalup, WA, Australia Received: June 18, 2013 Accepted after revision: November 18, 2013

Discrepancies exist whether blood flow restriction (BFR) exacerbates exercise-induced muscle damage (EIMD). This study compared low-intensity eccentric contractions of the elbow flexors with and without BFR for changes in indirect markers of muscle damage. Nine untrained young men (18–26 y) performed low-intensity (30% 1RM) eccentric contractions (2-s) of the elbow flexors with one arm assigned to BFR and the other arm without BFR. EIMD markers of maximum voluntary isometric contraction (MVC) torque, range of motion (ROM), upper arm circumference, muscle thickness and muscle soreness were measured before, immediately after, 1, 2, 3, and 4 days after exercise. Electromyography (EMG) amplitude of the biceps brachii and brachioradialis were recorded during exercise. EMG amplitude was not significantly different between arms and did not significantly change from set 1 to set 4 for the biceps brachii but increased for the brachioradialis (p ≤ 0.05, 12.0% to 14.5%) when the conditions were combined. No significant differences in the changes in any variables were found between arms. MVC torque decreased 7% immediately post-exercise (p ≤ 0.05), but no significant changes in ROM, circumference, muscle thickness and muscle soreness were found. These results show that BFR does not affect EIMD by low-intensity eccentric contractions. Keywords: muscle soreness, maximal voluntary contraction, electromyography, vascular occlusion, KAATSU

A novel form of resistance exercise utilizing low intensity (~20–30% one repetition maximum: 1RM) muscle contractions combined with blood flow restriction (BFR) has been shown to increase muscle mass and strength, and its effects are similar to those of high-intensity resistance exercise (14). BFR is documented to be beneficial for older adults or those unable or contraindicated to lift heavy loads (7, 17, 20). However, some studies report that when BFR resistance exercise is performed to failure, greater indices of muscle damage are produced compared to non-BFR exercise. Wernbom et al. (26) reported that low-intensity (30% of 1RM) knee extensor exercise to failure with BFR produced greater decreases in maximal voluntary contraction (MVC) torque immediately post-exercise (–62%) when compared to the non-BFR condition (–22%). In addition, there was a tendency that MVC torque remained below baseline at 72 hours (–10%) for the BFR condition. In contrast, Loenneke et al. (13) had participants exercise (30, 15, 15,

Corresponding author: Robert S. Thiebaud Department of Health and Exercise Science, University of Oklahoma 1401 Asp Ave., Norman, OK, 73019, USA Phone: +1-405-325-5211; Fax: +1- 405-325-0594; E-mail: [email protected] 0231–424X/$ 20.00 © 2014 Akadémiai Kiadó, Budapest

Blood flow restriction and muscle damage


15 reps) with and without BFR and found no significant decreases in muscle torque for either condition at 24 hours post-exercise. Some differences in the exercise and BFR protocols could have contributed to the different findings between studies, but it should be clarified whether BFR induces greater muscle damage than exercise without BFR. It has been reported that low-intensity resistance exercise combined with BFR produces greater muscle activation when compared with low-intensity resistance exercise alone (28). This increased activation may be associated with the muscle hypertrophy responses found with BFR resistance exercise. Yasuda et al. (29) found that muscle activation increased significantly over time for concentric actions but not for eccentric actions when combined with BFR. However, it is unknown if muscle activation would differ between eccentric actions with or without BFR and if muscle activation would affect the magnitude of muscle damage. When examining the concentric and eccentric component, one study reported that lower body concentric only exercise with BFR to failure produced greater levels of muscle soreness and decreases in maximum voluntary contraction (MVC) torque at 24 and 48 hours postexercise when compared to eccentric only exercise with BFR (22). It is known that muscle damage is induced by eccentric contractions and not by concentric contractions (8, 16), if no BFR is imposed. Our recent study compared eccentric only and concentric only arm curls with BFR using a submaximal protocol of 30, 15, 15, 15 repetitions and found significant increases in muscle soreness (20 mm, 0–100 mm visual analog scale) only after eccentric exercise with BFR (21). However, no significant changes in MVC torque, range of motion and swelling were found at 24 and 48 hours post-exercise for either conditions. It is not known whether the soreness produced in the eccentric only condition was due to the BFR or due to the eccentric contraction itself. It has been reported that low-intensity eccentric contractions do not induce muscle damage (4, 9); however, it is possible that low-intensity eccentric contractions with BFR induce muscle damage. It is therefore important to clarify if BFR increases the risk of muscle damage as it is recommended for older individuals and those recovering from injury. Thus, the purpose of this study was to examine the effects of BFR on indirect muscle damage markers and electromyography (EMG). We hypothesized that low-intensity eccentric contractions with BFR would result in greater changes in indirect markers of muscle damage than low-intensity eccentric exercise without BFR, and that muscle activation would not significantly increase in either condition. Materials and Methods Young men (n = 9) were recruited for this study, and their average age, body mass and body mass index (BMI) were 22.4 ± 3.2 years, 71.7 ± 16.8 kg, and 22.2 ± 3.4 kg/m2, respectively. Using G*Power 3.1.4, an a priori sample size estimation based on MVC torque found that 8 participants were needed for a potential difference between conditions with a moderate effect size of 0.4, an alpha level of 0.05 and power level of 0.80. Participants were recreationally active but had not participated in a resistance training program during the previous 6 months. Participants were excluded if they took anti-inflammatory medication, were hypertensive or had more than one risk factor for thromboembolisms (15). All procedures were approved by the university’s institutional review board. Prior to participation, participants were thoroughly informed of the purpose, all procedures, and tests of the study and signed a consent form. Acta Physiologica Hungarica 101, 2014


Thiebaud RS et al.

A cross-over study design was used with dominant and non-dominant arms of each participant randomly being assigned and counterbalanced to eccentric exercise with or without BFR with ~30 minutes between bouts. The week prior to the exercise session, participants were screened for exclusion criteria, filled out a consent form and a physical activity readiness questionnaire, and were familiarized with all testing procedures. The concentric 1RM was determined for each arm as the heaviest weight lifted through a concentric full range of motion (0°: a full extension to 130°: a full flexion) with proper form using standard 1RM procedures (1). The concentric 1RM was used in a previous study (21) that was the base for the present study, and it is practically used in a typical BFR training session. The average 1RM was 11.9 ± 3.6 kg for the dominant arm and 11.4 ± 1.6 kg for the non-dominant arm, without a significant difference between them. Participants returned the following week for the exercise session and measurements consisting of upper arm circumference, muscle thickness, range of motion (ROM), muscle soreness and maximum voluntary isometric contraction (MVC) torque were taken in this order before the exercise. The exercise session consisted of four sets (30, 15, 15, 15 repetitions) of free weight dumbbell curls with or without BFR at ~30% of their concentric 1RM with 30 seconds of rest between sets. During the exercise, the cadence was set at 2-s for eccentric actions with the arm slowly lowering the dumbbell from the elbow flexed (90°) to the elbow extended (0°) position. After each eccentric contraction, the dumbbell was returned to the starting position by the investigator. After exercise, MVC torque was measured within ~1–2 min after exercise, followed by measurements of upper arm circumference, muscle thickness, ROM and muscle soreness. Participants returned to the laboratory at 1, 2, 3, and 4 days postexercise for the measurements of the variables in the same order as that at pre-exercise. Upper arm circumferences were measured using a tape measure at 20%, 30%, 40% and 50% of upper arm length. Muscle thickness was measured at the same sites as those of the circumference measures using B-mode ultrasound (FF Sonic UF-4500, Fukuda Denshi, Tokyo, Japan) with a 5-MHz probe (21). Range of motion (ROM) was determined by subtracting the flexed from relaxed elbow joint angles using the average of the two measures. A visual analog scale (VAS 0–100 mm) with 0 mm indicating “no pain” and 100 mm indicating “very, very painful” (2) was used to assess the level of muscle soreness when the investigator passively flexed and extended the elbow joint. MVC torque of the elbow flexors were measured at 60° and 90° of elbow flexion on an isokinetic dynamometer (Biodex System 3 Isokinetic Dynamometer, USA). Participants performed 2 contractions each lasting 3 seconds and rested for 45 seconds between contractions with a 2-minute rest period between angles (60° and 90° in this order). The highest MVC of the two attempts for each angle was used for further analysis. For BFR, a specially designed elastic pressure cuff (3.3 cm × 58 cm) was placed around the most proximal part of the upper arm using the KAATSU Master device (Sato Sports Plaza, Japan). The initial cuff pressure when the cuff was placed around the arm prior to inflation was ~35 mmHg, and the pressure was gradually increased to a final pressure of 120 mmHg. Surface electrodes (Ag/AgCl electrode, QuitonQuik-Prep: Quiton Inc., USA) were placed on the line between the medial acromion and the fossa cubit at a distance of 1/3 from the fossa cubit for the biceps brachii. Surface electrodes were also placed at 20% of the distance between the fossa cubit and radial carpal joint for the brachioradialis and on the 7th cervical vertebrae for the ground electrode. The electrodes were connected to an electro­ myogram amplifier EMG 100C (Biopac System, Inc. Goleta, USA) and streamed through an analog to digital converter (Biopac System, Inc. Goleta, USA) to a lab computer (Dell Inc. Acta Physiologica Hungarica 101, 2014

Blood flow restriction and muscle damage


Round Rock, USA). The signals were low-pass filtered (cutoff at 500 Hz), high-pass filtered (cutoff at 10 Hz), and amplified 1000 times before being sampled at a rate of 1 KHz. Labview 7.1 (National Instrument Corporation, Austin, USA) was used to integrate the EMG signal. The EMG signal (RMS) was recorded during each MVC and during each repetition performed. The EMG amplitudes were normalized by the using the RMS value during MVC. All repetitions were normalised and the last six repetitions of each set were averaged and reported. A two-way repeated measures ANOVA (condition × time) was used to compare changes in the dependent variables between BFR (BFR-ECC) and non-BFR (ECC) conditions. When a significant time effect was found, follow-up testing was performed using pairwise comparisons with a Bonferroni adjustment. All values were expressed as mean ± SD. Statistical significance was set at p ≤ 0.05. Results No significant differences were found between BFR-ECC and ECC conditions for changes in any muscle damage markers (Table I). Maximum voluntary contraction torque at 60° significantly decreased by 7% immediately post-exercise but returned to the baseline by 24 hours post-exercise. MVC torque at 90° did not change significantly, and no significant changes over time were found for ROM, arm circumference, muscle thickness and muscle soreness. In the table, only the upper arm circumference and muscle thickness measured at 40% site are shown, but other sites (20%, 30%, and 50%) showed the same pattern. Table I. Indirect markers of muscle damage  



Day 1

Day 2

Day 3

Day 4


57.2 ± 16.4

54.0 ± 16.5*

56.3 ± 16.6

57.8 ± 15.5

57.8 ± 15.4

57.3 ± 15.8


57.2 ± 14.3

52.5 ± 13.1*

56.6 ± 16.3

57.4 ± 12.3

57.8 ± 15.3

58.4 ± 12.8


54.6 ± 15.2

51.9 ± 13.5

56.4 ± 15.8

57.4 ± 13.8

55.9 ± 16.1

55.9 ± 13.5


53.7 ± 11.9

51.2 ± 9.8

54.3 ± 13.3

57.8 ± 15.5

57.5 ± 15.4

58.5 ± 12.6


132.6 ± 7.9

130.9 ± 7.2

133.2 ± 7.3

133.7 ± 6.4

134.9 ± 6.8

135.1 ± 6.7


135.3 ± 6.3

133.0 ± 5.2

134.3 ± 7.5

134.7 ± 5.1

135.7 ± 7.8

135.8 ± 4.2


28.1 ± 3.3

28.5 ± 3.2

28.3 ± 3.0

28.2 ± 2.9

28.3 ± 3.0

28.4 ± 3.0


28.2 ± 3.7

28.3 ± 3.5

28.6 ± 3.4

28.5 ± 3.5

28.6 ± 3.3

28.5 ± 3.4


30.7 ± 4.1

30.9 ± 3.6

31.0 ± 4.7

30.8 ± 4.0

30.7 ± 4.1

31.2 ± 4.7


31.3 ± 4.3

31.0 ± 4.5

31.2 ± 4.2

31.6 ± 4.3

32.0 ± 4.6

31.6 ± 4.8


0.2 ± 0.4

1.8 ± 3.9

4.7 ± 5.0

2.8 ± 3.6

1.6 ± 3.0

0.1 ± 0.3


0.2 ± 0.4

1.2 ± 1.3

2.3 ± 2.3

1.0 ± 1.3

0.1 ± 0.3

0.2 ± 0.7

MVC @ 60° (Nm)

MVC @ 90° (Nm)

ROM (°)

Circumference (cm)

Thickness (mm)

Muscle soreness (mm)

Changes (mean ± SD) in maximum voluntary contraction torque (MVC) at 60° and 90°, range of motion (ROM), upper arm circumference and muscle thickness at 40% site, and muscle soreness before (Pre), immediately after (Post), and 1–4 days after eccentric exercise with blood flow restriction (BFR-ECC) and without blood flow restriction (ECC). *p < 0.05 from Pre Acta Physiologica Hungarica 101, 2014


Thiebaud RS et al.

Figure 1 shows the average EMG amplitude relative to the EMG amplitude during MVC for the last 6 eccentric contractions of each set over 4 sets. No significant differences were found between BFR-ECC and ECC conditions for the changes in EMG of either biceps brachii or brachioradialis. The EMG amplitude did not significantly change over sets for the 13 biceps brachii, but significantly increased from set 1 (12.0 %) to set 4 (14.5%) for the brachioradialis.

Fig. 1. Changes (mean ± SD) in EMG amplitude relative to the amplitude during maximal voluntary isometric Fig. 1. Changes (mean  SD) in EMG amplitude relative to the amplitude during ma contraction for biceps brachii (A) and brachioradialis (B) over 4 sets of eccentric contractions (last 6 contractions contraction biceps brachii of each set) without (ECC) and with blood flow restrictionfor (BFR-ECC). *p(A) < 0and .05brachioradialis from set 1 (B) over 4 sets of eccentric contra each set) without (ECC) and with blood flow restriction (BFR-ECC). *p < A és B ábrát egymás mellé kérem tördelni!


The present study tested the hypothesis that muscle damage would be induced by lowintensity eccentric contractions with BFR, and EMG activities of the elbow flexors would not be increased by BFR. Changes in any of the indirect markers of muscle damage and EMG were similar between BFR-ECC and ECC, and significant changes after exercise were found only for MVC at 60° (Table I). In addition, a small increase in EMG over sets was found only for the brachioradialis (Fig. 1). These results did not support the hypotheses. Fig. 1.ItChanges (mean reported  SD) in EMG amplitude the amplitude during maximal voluntarywhen isometric has been that little relative or no tomuscle damage is produced performing lowcontraction for biceps brachii contractions. (A) and brachioradialis over 4 sets ofLavender eccentric contractions (last 6 contractions of intensity eccentric For(B)example, and Nosaka (9) showed that lowset) withoutcontractions (ECC) and with blood flow restriction (BFR-ECC). *p < 0MVC, .05 from set 1 kg) did not change intensityeacheccentric of the elbow flexors (10% ~2.4 MVC force, ROM, upper arm circumference, plasma creatine kinase activity and muscle A és B ábrát egymás mellé kérem tördelni! soreness. However, in the same study, eccentric contractions with 40% MVC load (~9.7 kg) produced significant decreases in MVC force, and increases in upper arm circumference and muscle soreness. In the present study, the weight used for eccentric exercise was 30% of 1RM (3.5–3.6 kg) which was slightly heavier than the 10% MVC weight but much lighter than the 40% MVC weight (~9.7 kg) used in the study by Lavender and Nosaka (9). In the current study, only a small decrease in MVC torque at 60° (7%) was found at immediately post-exercise, and other variables did not change significantly (Table I). Therefore, it appears that BFR did not exacerbate muscle damage induced by the low-intensity eccentric contractions, as a previous study reported (21). Previous studies reported that some muscle soreness was developed after low-intensity exercise with BFR (21, 22). However, the current study did not find significant increases in Acta Physiologica Hungarica 101, 2014

Blood flow restriction and muscle damage


soreness following BFR exercise. Possible reasons for this discrepancy are due to differences in exercise protocols and the methods with which soreness was assessed between studies. Umbel et al. (22) found that BFR knee extension eccentric exercise performed to failure increased soreness to levels of 1.6 (0–10 scale). The total amount of repetitions performed in that study was considerably greater compared to the current study (137 reps. vs. 75 reps.) and time under BFR was longer (12 minutes vs. 5 minutes). Furthermore, participants retrospectively rated the soreness they had experienced with activities they had performed prior to coming into the laboratory for testing. Thiebaud et al. (21) used a similar exercise protocol (30, 15, 15, 15 reps.) and exercise load (~3.5 kg vs. ~3.6 kg) to the current study but found that soreness significantly increased to ~20 mm after BFR-ECC exercise using the same VAS as that used in the present study. In the study by Thiebaud et al. (21) participants palpated their upper arm to a depth of ~5 mm with their fingers while in the current study, the investigator passively flexed and extended the participant’s forearm and had the participants rate their soreness after both movements. Other studies have found higher levels of muscle soreness when performing BFR exercise to fatigue, although the levels of soreness were not significantly different from the non-BFR condition (24, 25). Therefore, performing exercise to failure may produce greater muscle soreness than performing a non-fatiguing protocol with BFR; however, it does not appear that severe delayed onset muscle soreness is developed because of BFR. It has been suggested that BFR may create an ischemia/reperfusion type injury that could elicit muscle damage beyond that of normal exercise (22). Ischemia/reperfusion injury occurs after complete occlusion of blood flow to skeletal muscle and increases lactic acid, hydrogen ions, intracellular calcium, reactive oxygen species, and eventually if sustained for a prolonged period, cell necrosis (23). Yet, it seems unlikely that all of these events are happening in BFR low-intensity eccentric contractions. First, the current study most likely did not completely occlude blood flow as a moderate pressure of 120 mmHg was used. Although blood flow was not measured, other studies have found that a pressure of 160 mmHg does not cut off arm blood flow but a pressure of 300 mmHg does (27, 28). Secondly, high levels of reactive oxygen species may not be produced with BFR. For instance, after performing leg extensions with BFR to fatigue, neither plasma creatine nor lipid peroxides levels significantly increased (19). In addition, one study observed that markers of oxidative stress (protein carbonyls and blood glutathione status) were not increased after BFR exercise, although the markers increased during BFR alone (5). It is plausible that if a higher intensity was used, a more substantial difference may have been found between conditions. It has been shown that the higher the intensity of eccentric contractions, the greater the magnitude of muscle damage induced (3). Higher intensity contractions could also produce more fatigue resulting in increased mechanical damage and could potentially increase the inflammatory and oxidative response leading to more muscle damage. Therefore, the low-intensity model used in this study may not have been ideal to determine any negative effects of BFR. However, in terms of practical use and the purpose of BFR, low-loads (20–30% 1RM) are used to decrease the mechanical stress on joints and muscles. Hence, the low-intensity eccentric exercise used in the current study more accurately reflects the type of stimulus that may be experienced during BFR exercises. Another important point to consider with BFR exercise is the amount of blood flow restriction in the limb. Research suggests that the size of the limb directly impacts the arterial occlusion pressure in the lower body; therefore, the use of an arbitrary pressure is a limitation in the current study (11). If the restrictive pressure is too great, complete occlusion may occur Acta Physiologica Hungarica 101, 2014


Thiebaud RS et al.

and possibly produce more muscle damage. However, if the restriction pressure is not enough, significant muscle swelling may not occur. This is a key consideration because it has been proposed that muscle swelling may be a significant stimulate of muscle growth with BFR (10, 12). In the current study, little muscle swelling was found following BFR-ECC exercise. Because of this, the set pressure of 120 mmHg which was used for all participants may not have been sufficient enough for some participants resulting in non-significant changes in muscle thickness post-exercise. It is known that eccentric contractions are a more potent stimulus for muscle hypertrophy than concentric contractions (6, 18). Therefore, it is possible that eccentric contractions with BFR would be more effective for muscle hypertrophy and strength gains than eccentric contractions alone. It is interesting to note that muscle activity during the low-intensity eccentric contractions was not affected by BFR (Fig. 1), although previous studies have shown that BFR increases muscle activity during concentric contractions (25, 28). Yasuda et al. (29) reported that muscle hypertrophy was different between concentric and eccentric contraction training with BFR after 6 weeks. They found that muscle CSA increased at the mid-upper arm and 10 cm above the elbow joint after concentric contraction training with BFR. However, muscle CSA only increased at 10 cm above the elbow joint after eccentric contraction training with BFR. Therefore, it is possible that less muscle hypertrophy resulted due to the whole muscle not being activated by eccentric contractions with BFR. It should be investigated further whether eccentric contractions with BFR are more beneficial for muscle hypertrophy and strength gain than eccentric contractions without BFR or volume matched concentric contractions with BFR. In conclusion, low-intensity eccentric contractions of the elbow flexors with BFR do not induce muscle damage. However, performing low-intensity BFR-ECC exercise may not be a strong stimulus to promote muscle hypertrophy due to low muscle activation levels and little muscle swelling. Future studies should investigate how different BFR cuff pressures or how different exercise protocols with different intensities and number of contractions may affect the muscle damage response and training outcomes. Acknowledgements The authors would like to thank Dr. Travis Beck and Dr. Jason DeFreitas for their assistance with EMG data collection and analysis.

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Acta Physiologica Hungarica 101, 2014

Muscle damage after low-intensity eccentric contractions with blood flow restriction.

Discrepancies exist whether blood flow restriction (BFR) exacerbates exercise-induced muscle damage (EIMD). This study compared low-intensity eccentri...
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