European Journal of Applied Physiology

https://doi.org/10.1007/s00421-019-04095-9

ORIGINAL ARTICLE

Damage protective effects conferred by low-intensity eccentric

contractions on arm, leg and trunk muscles
Min‑Jyue Huang1 · Kazunori Nosaka2 · Ho‑Seng Wang1 · Kuo‑Wei Tseng3 · Hsin‑Lian Chen4 · Tai‑Ying Chou5 ·
Trevor C. Chen1

Received: 8 October 2018 / Accepted: 6 February 2019

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract
Purpose Low-intensity eccentric contractions with a load corresponding to 10% of maximal voluntary isometric contrac-
tion strength (10% EC) attenuate muscle damage in a subsequent bout of higher-intensity eccentric contractions performed
within 2 weeks for the elbow flexors, knee flexors and knee extensors. However, it is not known whether this strategy could
be applied to other muscles. This study investigated whether 10% EC would confer damage protective effect on high-intensity
eccentric contractions (80% EC) for nine different muscle groups.
Methods Untrained young men were placed to an experimental or a control group (n = 12/group). Experimental group
performed 50 eccentric contractions with a load corresponding to 10% EC at 2 days prior to 50 eccentric contractions with
80% EC for the elbow flexors and extensors, pectoralis, knee flexors and extensors, plantar flexors, latissimus, abdominis
and erector spinae. Control group performed 80% EC without 10% EC. Changes in maximal voluntary isometric contraction
strength (MVC) and muscle soreness, plasma creatine kinase (CK) activity and myoglobin concentration after 80% EC were
compared between groups by a mixed-factor ANOVA.
Results MVC recovered faster (e.g., 6–31% greater MVC at 5 days post-exercise), and peak muscle soreness was 36–54%
lower for Experimental than Control group for the nine muscles (P < 0.05). Increases in plasma CK activity and myoglobin
concentration were smaller for Experimental (e.g., peak CK: 2763 ± 3459 IU/L) than Control group (120,360 ± 50,158 IU/L).
Conclusions These results showed that 10% EC was effective for attenuating the magnitude of muscle damage after 80% EC
for all muscles, although the magnitude of the protective effect differed among the muscles.

Keywords Lengthening contraction · Delayed-onset muscle soreness · Maximal isometric contraction strength · Creatine
kinase · Rhabdomyolysis

Abbreviations
Communicated by William J. Kraemer. ANOVA Analysis of variance
CK Creatine kinase
* Trevor C. Chen CV Coefficient of variation
[email protected] DOMS Delayed-onset muscle soreness
1
Department of Physical Education, National Taiwan EC Eccentric contractions
Normal University, P.O. Box 97‑71, Wenshan Wansheng, ECM Extracellular matrix
Taipei 11699, Taiwan, Republic of China MVC Maximal voluntary isometric contraction
2
Centre for Exercise and Sports Science Research, School R Intraclass correlation coefficient
of Medical and Health Sciences, Edith Cowan University, SD Standard deviation
Western Australia, Australia
3
Department of Exercise and Health Sciences, University
of Taipei, Taipei, Taiwan, Republic of China Introduction
4
Department of Physical Education, Health
and Recreation, National Chiayi University, Chiayi, Unaccustomed eccentric exercise induces muscle dam-
Taiwan, Republic of China
age represented by a prolonged loss of muscle function,
5
Department of Athletic Performance, National Taiwan delayed-onset muscle soreness (DOMS), and elevation of
Normal University, Taipei, Taiwan, Republic of China

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 European Journal of Applied Physiology

muscle proteins such as creatine kinase (CK) and myoglo- Methods

bin in the blood (Hyldahl and Hubal 2014; Lin et al. 2018;
Tsuchiya et al. 2018). Thus, when prescribing eccentric Participants
exercise to novice individuals, caution is required for
possible severe muscle damage that may result in serious Twenty-four untrained healthy university students pro-
consequences such as rhabdomyolysis (O’Connor et al. vided informed consent to participate in the study that
2008; Hubal et al. 2010; Rawson et al. 2017). One of the had been approved by the Research Ethics Committee
effective strategies to minimize muscle damage is to pre- of National Taiwan Normal University, Taiwan, and an
condition muscles by low-intensity eccentric contractions informed consent was obtained from each participant. The
prior to higher-intensity eccentric contractions (Chen et al. study was conducted in conformity with the policy state-
2012; Lin et al. 2015). ment regarding the use of human subjects by the 1964
Chen et al. (2012) reported that performing 30 low- Declaration of Helsinki. Their mean (± SD) age, height,
intensity eccentric contractions (EC) with a dumbbell cor- and body mass were 21.6 ± 1.8 years, 172.4 ± 5.9 cm, and
responding to 10% of maximal voluntary isomeric contrac- 68.8 ± 11.8 kg, respectively. The sample size was esti-
tion (MVC) strength (10% EC) enhanced the recovery of mated using the data from a previous study (Chen et al.
MVC strength at 1–4 days post-exercise by 18–59%, reduced 2012) in which the protective effect of 10% EC on 100%
peak muscle soreness by 66%, and decreased peak plasma EC was investigated for the elbow flexors. Based on the
CK activity by 74% after 30 maximal eccentric contractions effect size of 1 for a possible difference in MVC strength
(100% EC) of the unilateral elbow flexors performed by the changes between the conditions with and without 10% EC,
same arm 2 days later. A similar protective effect of 10% it was estimated that at least 8 participants were neces-
EC on muscle damage after 100% EC was also shown for sary for each condition, with the alpha level of 0.05 and
the knee flexors and knee extensors (Lin et al. 2015). How- power (1 − β) of 0.80, using G*Power (G*Power 3.1.9.2,
ever, practical applications of this to resistance exercises Heinrich-Heine-Universitat Dusseldorf, Dusseldorf, Ger-
performed in a gym have not been explored. many; http://www.gpowe​r.hhu.de/). The participants were
It has been reported that the magnitude of muscle damage placed into a control or an experimental group (n = 12/
is greater for arm than leg muscles after maximal eccen- group) by matching the baseline MVC strength of the nine
tric contractions performed on an isokinetic dynamometer muscles as much as possible. No significant differences in
(Jamurtas et al. 2005; Paschalis et al. 2010; Chen et al. age [P = 0.099, Cohen’s d (d) = 0.786], height (P = 0.166,
2011). Hyldahl et al. (2017) reported that the magnitude d = 0.461), body mass (P = 0.302, d = 0.289), MVC
of the repeated bout effect was greater for the elbow flexors strength of all muscles (latissimus: P = 0.060, d = 0.647—
than knee extensors. However, no previous study has com- elbow extensors: P = 0.481, d = 0.451), and other baseline
pared arm, leg and trunk muscles for the protective effect values of the dependent valuables (e.g., muscle soreness:
in a practical setting. General guidelines for healthy adults P = 1.000) were observed between the groups.
include 8–10 resistance exercises targeting different muscle A familiarization session was set at 3 days prior to the
groups (American College of Sports Medicine 2009). Cur- first eccentric exercise session, in which the participants
rently, these exercises do not necessarily emphasize eccen- experienced the muscle soreness assessments, and per-
tric contractions. However, considering the potent effects of formed submaximal isometric contractions at the middle
eccentric resistance training on muscle and physical func- angle of the whole range of motion for each exercise. The
tion, insulin sensitivity and blood lipid profile found for investigator demonstrated the nine eccentric exercises.
older and young adults (Paschalis et al. 2011; Chen et al.
2017a, b), it is possible that eccentric contractions are more
emphasized in training routines. Study design
Therefore, the present study investigated the effect of
10% EC on muscle damage induced by higher-intensity The experimental group performed 10% EC (5 sets of 10
eccentric contractions for arm, leg and trunk muscles; the contractions) for each of nine resistance exercises; arm
elbow flexors, elbow extensors, pectoralis, knee flexors, curl (targeted muscle: elbow flexors), elbow extension
knee extensors, plantar flexors, latissimus, abdominis, and (elbow extensors), chest press (pectoralis), leg extension
erector spinae involved in nine different resistance exercises (knee extensors), leg curl (knee flexors), standing calf raise
using machines equipped in a gym. It was hypothesized that (plantar flexors), lat pulldown (latissimus), abdominal
the 10% EC would confer potent muscle damage protective crunch (abdominis), and back extension (erector spinae)
effect on all muscles, but the magnitude of the effect would in a counterbalanced order among the participants in the
be different among the muscles such that the effect would same day. These exercises were followed 2 days later by
be less for leg than arm muscles.

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5 sets of 10 eccentric contractions for each exercise with and exercises, and the time taken for the measurements was
a heavier load corresponding to 80% MVC strength (80% approximately 4 h.
EC). The control group performed the 80% EC of the nine
exercises without 10% EC. Dependent variables

Eccentric exercise The dependent variables consisted of MVC strength, muscle

soreness, and plasma CK activity and myoglobin concentra-
The 10% EC and 80% EC of nine eccentric exercises were tion. The re-test reliability based on intraclass correlation
performed on nine commercially available resistance train- coefficient (R) and coefficient of variation (CV) of MVC
ing machines (Cybex International, Inc., Owatonna, MN, strength and muscle soreness for the nine muscles was
USA) set in a gym of the university. Most of the machines 0.82–0.94, and 8.4–9.8%, and 1.00 and 0%, respectively. R
such as those for the arm extension, chest press, leg exten- and CV were 0.73 and 9.7% for CK, and 0.75 and 8.7% for
sion, leg curl, standing calf raise, lat pulldown and abdomi- myoglobin.
nal crunch included a cam system (https​://www.cybex​intl.
com/sitem​ap-menu.aspx). To determine the load for each Maximal voluntary isometric contraction strength
exercise, maximal voluntary isometric contraction (MVC)
strength of each targeted muscle was measured on each MVC strength of the nine corresponding muscles was meas-
resistance exercise machine using a loadcell (model: SESB, ured by the load cell system explained above. The measure-
Delta-Transducer Inc., CA, USA) that was implemented to ments were taken twice with a 45-s rest between measures,
each machine, and connected to an A/D system (MP150 and the highest value of the two was used for further analysis
Data Acquisition and Analysis System, Biopac Systems Inc., (Wang et al. 2014; Chen et al. 2015; Shih et al. 2016). For
CA., USA). The joint angle for the MVC strength measure the arm and leg muscles, MVC strength was measured for
was at 90° of elbow flexion for the elbow flexors, elbow both limbs together. It should be noted that the cam sys-
extensors, pectoralis and latissimus, 70° and 40° of knee tem used in the machines affected the MVC strength val-
flexion for the knee extensors and knee flexors, respectively, ues, resulting in greater values than those measured by an
0° of plantar flexion for the plantar flexors, and 50° and 40° isokinetic dynamometer or other devices that assess MVC
of trunk flexion for the abdominis and erector spinae, respec- strength.
tively. The participants were asked to generate maximal vol-
untary isometric force for 5 s, and this was repeated twice Muscle soreness
with a 45-s rest between attempts. The peak value during the
5-s contraction was recorded, and the highest value of the Muscle soreness was quantified by a visual analog scale
two peak values was used to determine the loading weight that had a 100-mm continuous line with “not sore at all”
(80% of MVC strength). on one end (0 mm) and “very, very sore” on the other end
Each contraction lasted for 5 s guided by the investigator (100 mm). Muscle soreness of each muscle for the right and
who counted “0, 1, 2, 3, 4, 5” for the movement. The par- left sides as well as the trunk muscles was assessed, sepa-
ticipants were instructed to resist the load for whole range of rately, when each muscle was self-stretched for the maximal
motion for each exercise. The starting and finishing angles (Nelson and Kokkonen 2014).
of each exercise were 120°–0° for the arm curl, 0°–120° for
the elbow extension, 0°–90° of elbow flexion for the chest Plasma CK activity and myoglobin concentrations
press, 110°–0° for the leg curl, 0°–110° for the leg extension,
40° of plantar flexion − 25° of dorsiflexion for the calf raise, Approximately 5 ml of venous blood was withdrawn by
90°–0° of elbow flexion for the lat pulldown, 90°–0° of trunk a standard venipuncture technique from the cubital fossa
flexion for the abdominal crunch, and 0°–90° trunk flexion region and centrifuged for 10 min to extract plasma, and
for the back extension. After each eccentric contraction at the plasma samples were stored at − 80 °C until analyses.
the end of the range of motion, the investigator assisted to Plasma CK activity was assayed spectrophotometrically
set the load to the starting position while the participants by an automated clinical chemistry analyser (Model 7080,
were instructed to relax their muscles. The interval between Hitachi, Co. Ltd., Tokyo, Japan) using a commercial test kit
contractions was 15 s, and a 2-min rest between sets was (Roche Diagnostics, Indianapolis, USA). Plasma myoglobin
provided. Participants performed the eccentric contractions concentration was measured by an automated clinical chem-
as instructed, but when they had difficulty controlling the istry analyser (Model Elecsys 2010, F. Hoffmann-La Roche
eccentric contractions in 80% EC, the investigator spot- Ltd., Tokyo, Japan) using a commercial test kit (Roche Diag-
ted to assist the movement. The total duration of the whole nostics, Indianapolis, USA) (Tseng et al. 2016; Chen et al.
exercise session including the resting time between sets 2018a).

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Index of protection (P = 0.535, d = 0.670) before 80% EC were observed

between the groups. However, the baseline value of plasma
The magnitude of the protective effect (index of protection) CK activity before 80% EC was higher (P = 0.019, d = 0.960)
was calculated using the following equation: (80% EC of the for the experimental (336 ± 270 IU/L) than control group
control group – 80% EC of the experimental group) / 80% (153 ± 11 IU/L).
EC of the control group × 100 (Chen et al. 2014, 2016). For Figure 1 compares the experimental and control groups
MVC, the values at 2 days post-exercise were used, and peak for normalized changes in MVC strength of the nine mus-
values were used for muscle soreness, plasma CK activity cles after 80% EC. A significant interaction effect was found
and myoglobin concentration. (P < 0.001, η2 = 0.457), and MVC strength recovered faster
for the experimental than control group for all muscles
Statistical analysis (latissimus: P < 0.001, η2 = 0.321—abdominis: P < 0.001,
η2 = 0.659).
All dependent variables before the 10% EC and 80% EC of Muscle soreness developed less for the experimental than
the experimental group and 80% EC of the control group control group for all nine muscles (pectoralis: P < 0.006,
were compared by t tests. Changes in MVC strength and η2 = 0.249—abdominis: P < 0.001, η2 = 0.703) as shown
soreness of each muscle over time following 10% EC or in Fig. 2. The peak soreness values of the nine muscles of
80% EC were compared by a repeated-measure of one-way the experimental group (3 ± 8–29 ± 26 mm) was 8–54%
analysis of variance (ANOVA). Changes in the dependent smaller (knee extensors: P = 0.001, d = 0.841—erector spi-
variables after 80% EC were compared between the groups nae: P < 0.001, d = 1.595) than those of the control group
by a mixed-design of two-way ANOVA. When a significant (42 ± 24–73 ± 22 mm).
interaction effect was found, a Tukey’s post hoc test was Changes in plasma CK activity (P < 0.001, η2 = 0.780)
performed. The effect size for the difference in each variable and myoglobin concentration (P < 0.001, η2 = 0.802) were
between the experimental and control groups was calculated smaller for the experimental than control group (Fig. 3).
using Cohen’s d (d), and the effect size was considered as Peak plasma CK activity (2763 ± 3459 IU/L) and myoglobin
small (d = 0.2), medium (d = 0.5), and large (d = 0.8), respec- concentration (185 ± 228 µg/L) of the experimental group
tively (Cohen 1988). Eta-squared values (η2) were also cal- were smaller (peak CK: P < 0.001, d = 1.694; peak myoglo-
culated as measures of effect size when ANOVA was per- bin: P < 0.001, d = 1.869) than those of the control group
formed, and a value of ~ 0.02 was considered as a small (120,360 ± 50,158 IU/L, 3418 ± 687 µg/L).
effect, ~ 0.13 as a medium effect, and > 0.26 as a large effect
(Bakeman 2000). A significant level was set at P ≤ 0.05. The The magnitude of the protective effect conferred
data were presented as mean ± standard deviation (SD). by 10% EC

The protective index ranges 43% (knee flexors)—75%

Results (erector spinae) for MVC strength, and 46% (knee exten-
sors)—92% (abdominis) for muscle soreness (Fig. 4). The
Changes in dependent variables after 10% EC protective index for MVC strength was the lowest for knee
flexors (43%), and the protective index for muscle soreness
No significant changes in MVC strength (elbow exten- was the lowest for knee extensors (46%) among the mus-
sors: P = 0.052, η 2 = 0.206—knee flexors: P = 0.860, cles. The average of the index of the nine muscles for MVC
η 2 = 0.022) and muscle soreness (elbow extensors: strength (59 ± 12%) was not different (P = 0.428, d = 0.751)
P = 0.060, η2 = 0.285—pectoralis: P = 0.698, η2 = 0.014) from that of the muscle soreness (69 ± 16%). The magnitude
of the nine muscles, and plasma myoglobin concentration of the protective effect for peak plasma CK activity and myo-
(P = 0.234, η2 = 0.124) were observed after 10% EC. How- globin concentration was 98% and 96%, respectively.
ever, plasma CK activity increased (P = 0.042, η2 = 0.250)
at 1 (268 ± 152 IU/L) and 2 days (336 ± 270 IU/L) after 10%
EC (Table 1). Discussion

Changes in dependent variables after 80% EC The results demonstrated that the 10% EC was effective for
enhancing the recovery of MVC strength (Fig. 1), and atten-
No significant differences in the baseline MVC strength uating the magnitude of muscle soreness (Fig. 2) for all nine
(elbow flexors: P = 0.089, d = 0.586—plantar flex- muscles. However, the magnitude of the protective effect
ors: P = 0.412, d = 0.130), soreness of the nine muscles conferred by the 10% EC was different among the muscles.
(P = 1.000, d = 1.000), and plasma myoglobin concentration The 10% EC largely reduced the increases in plasma CK

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European Journal of Applied Physiology

Table 1  Changes in maximal voluntary isometric contraction (MVC) (ABD), and erector spinae (ES), and plasma creatine kinase (CK)
strength and muscle soreness (Soreness) of the elbow flexors (EF), activity and myoglobin (Mb) concentration before (Pre), immediately
elbow extensors (EE), pectoralis (PEC), knee extensors (KE), knee after (Post), and 1 and 2 days after the 10% eccentric exercise
flexors (KF), plantar flexors (PF), latissimus dorsi (LAT), abdominis

Variables Pre Post 1 day 2 days

MVC (kg)
EF 51.0 ± 4.8 (48.0–54.1) 50.0 ± 4.9 (46.8–53.1) 51.1 ± 4.8 (48.0–54.2) 50.6 ± 4.8 (47.6–53.6)
EE 46.0 ± 4.5 (43.2–48.9) 44.6 ± 4.7 (41.7–47.6) 45.0 ± 4.1 (42.4–47.6) 45.8 ± 5.1 (42.5–49.0)
PEC 101.7 ± 7.7 (96.7–106.6) 100.9 ± 8.4 (95.5–106.2) 102.6 ± 7.9 (97.1–107.6) 100.8 ± 8.2 (95.6–106.0)
KE 159.9 ± 14.4 (150.7–169.1) 159.4 ± 14.8 (150.0–168.8) 160.2 ± 13.9 (151.3–169.1) 159.8 ± 13.7 (151.1–168.5)
KF 77.7 ± 7.0 (73.2–82.1) 76.8 ± 9.2 (71.0–82.7) 76.7 ± 7.9 (71.7–81.7) 77.1 ± 8.7 (71.6–82.6)
PF 125.1 ± 11.5 (117.8–132.4) 124.1 ± 14.9 (114.6–133.6) 122.9 ± 13.8 (114.2–131.7) 125.4 ± 13.2 (116.9–133.8)
LAT 63.9 ± 6.3 (59.9–67.9) 63.0 ± 6.5 (58.9–67.1) 63.5 ± 7.0 (59.0–67.9) 63.9 ± 7.0 (59.5–68.4)
ABD 87.9 ± 8.0 (82.8–93.0) 87.1 ± 8.0 (82.1–92.2) 87.9 ± 8.1 (82.8–93.1) 88.1 ± 8.7 (82.6–93.7)
ES 148.5 ± 13.4 (140.0–157.0) 147.9 ± 13.6 (139.2–156.6) 148.9 ± 12.8 (140.8–157.1) 149.2 ± 14.0 (140.3–158.1)
Soreness (mm)
EF 0.0 ± 0.0 (0.0–0.0) – 0.8 ± 2.9 (1.0–2.7) 0.0 ± 0.0 (0.0–0.0)
EE 0.0 ± 0.0 (0.0–0.0) – 6.3 ± 9.2 (0.5–12.2) 4.2 ± 7.9 (0.9–9.2)
PEC 0.0 ± 0.0 (0.0–0.0) – 0.9 ± 3.2 (1.1–2.9) 0.5 ± 1.4 (0.4–1.4)
KE 0.0 ± 0.0 (0.0–0.0) – 0.0 ± 0.0 (0.0–0.0) 0.1 ± 0.3 (0.1–0.3)
KF 0.0 ± 0.0 (0.0–0.0) – 1.1 ± 3.8 (1.4–3.5) 0.7 ± 2.3 (0.8–2.1)
PF 0.0 ± 0.0 (0.0–0.0) – 0.0 ± 0.0 (0.0–0.0) 0.0 ± 0.0 (0.0–0.0)
LAT 0.0 ± 0.0 (0.0–0.0) – 0.9 ± 0.8 (1.1–2.9) 0.8 ± 2.6 (0.9–2.4)
ABD 0.0 ± 0.0 (0.0–0.0) – 1.1 ± 3.8 (1.3–3.5) 0.7 ± 2.3 (0.8–2.1)
ES 0.0 ± 0.0 (0.0–0.0) – 0.0 ± 0.0 (0.0–0.0) 0.0 ± 0.0 (0.0–0.0)
CK (IU/L) 168.1 ± 16.0 (157.9–178.3) – 268.4 ± 152.0* (171.8–365.0) 335.5 ± 269.9* (164.0–507.1)
Mb (µg/L) 23.9 ± 1.2 (23.1–24.7) – 18.4 ± 9.6 (12.3–24.5) 24.2 ± 8.7 (18.7–29.7)

Values are means ± SD (95% confidence interval)

*Significant (P < 0.05) differences from the pre-exercise values. Values are means ± SD (95% confidence interval). *Significant (P < 0.05) differ-
ences from the pre-exercise values. MVC strength of EF, EE, PEC, KE, KF and PF was measured with both limbs together

activity and myoglobin concentration after 80% EC (Fig. 3). the first to show that this was also the case for the elbow
These results supported the hypothesis and showed that the extensors, pectoralis, plantar flexors, latissimus, abdominis
10% EC conferred potent protective effect on all muscles. and erector spinae. It appears that muscle damage can be
The differences in the MVC strength changes follow- attenuated by 10% EC performed 2 days prior to 80% EC for
ing 80% EC between the groups were most likely due to all muscles. However, the magnitude of the protection was
the preconditioning effect conferred by the 10% EC per- different among the muscles such that the protective effect
formed 2 days before the 80% EC. The recovery of MVC on MVC was greater for erector spinae (75%) and latissimus
strength at 2 days post-exercise was greater by 43% (knee (73%) than the knee extensors (45%) and knee flexors (43%),
flexors)—75% (erector spinae) for the experimental than while that on DOMS was greater for abdominis (92%), latis-
control group. No previous study has reported changes in simus (87%), plantar flexors (77%), erector spinae (72%) and
MVC strength following eccentric exercise of the elbow the elbow flexors (70%) in comparison to the knee extensors
extensors, pectoralis, plantar flexors, latissimus, abdominis (46%) and pectoralis (51%).
and erector spinae with a preconditioning exercise, although The 10% EC did not induce muscle soreness for any
three previous studies reported the effect of 10% EC on the of the muscles. This is consistent with the findings of the
elbow flexors (Chen et al. 2012, 2013), and the knee flexors previous studies (Chen et al. 2012, 2013, 2018b; Lin et al.
and knee extensors (Lin et al. 2015). It should be noted that 2015). For example, Chen et al. (2012) reported that peak
these previous studies used a unilateral eccentric exercise, muscle soreness was 66% less when 10% EC was performed
but bilateral eccentric exercises were performed in the pre- 2 days prior to 100% EC of the unilateral elbow flexors. In
sent study. Despite this difference, the findings of the present the present study, the magnitude of the protective effect on
study were in line with those of the previous studies (Chen muscle soreness conferred by 10% EC was 70%, 73% and
et al. 2012, 2013; Lin et al. 2015). The present study was 46% for the elbow flexors, knee flexors and knee extensors,

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Fig. 1  Normalized changes (mean ± SD) in maximal voluntary iso- 4 and 5 days after 80% eccentric exercise for the control group (Con)
metric contraction (MVC) strength of the elbow flexors (a), elbow and the experimental group (Exp). An asterisk (*) indicates a signifi-
extensors (b), pectoralis (c), knee extensors (d), knee flexors (e), cant difference (P < 0.05) between groups based on the interaction
plantar flexors (f), latissimus (g), abdominis (h), and erector spinae (i) effect shown by the ANOVA
from the baseline (pre: 100%), immediately after (post), and 1, 2, 3,

respectively. The extent of the protection for other muscles (Rawson et al. 2017). Thus, it may be that myoglobin also
was 58% for the elbow extensors, 51% for pectoralis, 77% for increased, but already retuned to the baseline by the time
plantar flexors, 87% for latissimus, 92% for abdominis and when the measurement was taken at 1 and 2 days post-10%
72% for erector spinae. The magnitude of the protection on EC. As shown in Fig. 3, plasma CK activity and myoglobin
the trunk muscles seemed greater than that of the arm and concentration did not increase significantly after 80% EC
leg muscles. It has been suggested that the greater protec- for the experimental group. This suggests that the 10% EC
tion could be conferred, if the muscles are less exposed to abolished the responses of plasma CK activity and myo-
eccentric contractions in daily activities (Chen et al. 2011). globin concentration following 80% EC. Peak plasma CK
This may explain the greater effect for the trunk muscles. activity and myoglobin concentration were 98% and 96%
Plasma CK activity increased after 10% EC, but plasma smaller, respectively, for the experimental than control group
myoglobin concentration did not. The molecular weight of in the present study. These effects seem to be greater than
myoglobin is 17.8 kDa, and its half-life is 1–3 h when glo- those found for the unilateral elbow flexors (peak CK: 74%,
merular filtration rate is normal, while the molecular weight myoglobin: 60%), knee extensors (78%, 71%) and knee flex-
of CK is about 81 kDa and its half-life is approximately 36 h ors (76%, 75%), in which 10% EC (elbow flexors and knee
(Beetham 2000). CK is primarily cleared by the reticulo- flexors: 30 repetitions, knee extensors: 60 repetitions) were
endothelial system, but myoglobin is cleared by the kidneys performed 2 days before 100% EC (Chen et al. 2012; Lin

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Fig. 2  Changes (mean ± SD) in muscle soreness assessed by a 100- 1, 2, 3, 4 and 5 days after the 80% eccentric exercise for the control
mm visual analog scale of the elbow flexors (a), elbow extensors (b), group (Con) and the experimental group (Exp). An asterisk (*) indi-
pectoralis (c), knee extensors (d), knee flexors (e), plantar flexors (f), cates a significant difference (P < 0.05) between groups based on the
latissimus (g), abdominis (h), and erector spinae (i) before (pre), and interaction effect shown by the ANOVA

Fig. 3  Changes (mean ± SD)

in plasma creatine kinase (CK)
activity and myoglobin (Mb)
concentration before (pre), and
1, 2, 3, 4 and 5 days after 80%
eccentric exercise for the control
group (Con) and the experimen-
tal group (Exp). An asterisk (*)
indicates a significant difference
(P < 0.05) between exercises
based on the interaction effect
shown by the ANOVA

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The mechanisms underpinning the protection conferred

by low-intensity eccentric contractions on higher-intensity
eccentric contractions are not clear yet, but the findings of
the current study provide some clues. Hyldahl et al. (2017)
have speculated that the protective effect is a combination
of neural adaptations, muscle–tendon complex behavior
changes, extracellular matrix (ECM) structural remodeling,
and modified inflammatory responses. Since the 10% EC
was performed only 2 days before the 80% EC, it seems
unlikely that any of structural adaptations were main con-
tributors. It is possible that the protection conferred by 10%
EC was more associated with neural adaptations such as
increased recruitment of slow-twitch motor units and activa-
tion of larger motor unit pool than adaptations at muscle fib-
Fig. 4  Index of protective effect of maximal isometric contraction ers and ECM. It is also possible that inflammatory responses
strength (MVC) and muscle soreness (SOR) of the elbow flexors were modified by the 10% EC as if an inoculation effect that
(EF), elbow extensors (EE), pectoralis (PEC), knee extensors (KE), triggers the immune system to be better prepared for upcom-
knee flexors (KF), plantar flexors (PF), latissimus (LAT), abdominis
(ABD), and erector spinae (ES). The index was calculated by the fol-
ing events. Yamada et al. (2018) have recently reported that
lowing formula: (80% EC of Con—80% EC of Exp)/80% EC of Con 10 non-damaging eccentric contractions performed 2 days
× 100%, for the magnitude of the decrease in MVC from the baseline prior to 100 maximal eccentric contractions of rat medial
at 2 days post-exercise and peak muscle soreness using the average gastrocnemius muscle improved contractile recovery, and
value of the group. The average and standard deviation values of the
nine muscles are also included as “Mean”
this was associated with a heat shock protein-dependent
prevention of immune cell invasion resulting in decreased
myeloperoxidase-mediated reactive oxygen species produc-
et al. 2015). It should be noted that the peak plasma CK tion, avoiding cell membrane disruption, calpain activation
activity for the control group in the present study (average and degenerative changes in myosin and actin molecules.
peak: 120,360 IU/L) was much greater than that of the pre- Regarding the differences in the magnitude of the protec-
vious study (6226 IU/L) (Chen et al. 2016). This was likely tive effect among the muscles, it should be noted that the
due to the use of more muscles in one session than that of range of motion in the nine exercises did not necessarily
the previous studies (Chen et al. 2011, 2016). It seems pos- induce similar sarcomere or muscle fiber strain among the
sible that the cumulative effect from different muscles made nine muscles. Thus, mechanical stress to each muscle was
the protective effect on plasma CK activity and myoglobin likely to be different, which resulted in different magnitude
in the present study greater than that of the previous stud- of muscle damage after 80% EC, and different magnitude
ies (Chen et al. 2012; Lin et al. 2015). It should be noted of the protective effect. It is interesting to investigate the
that muscle proteins in the blood increase largely after per- effect of 10% EC on 80% EC among different muscles by
forming several eccentric exercises of different muscles in matching the decrease in MVC at immediately post-exer-
a session, which is a risk of rhabdomyolysis. In the present cise. Definitely, further studies are required to elucidate the
study, many of the participants in the control group had dark mechanisms of the protection.
urine after the session, showing a symptom of rhabdomy- The present study provides important practical implica-
olysis, although no serious case was developed. It seems tions. Performing low-intensity eccentric contractions was
unlikely that the exercises used in the present study (5 sets effective for preventing severe muscle damage. Thus when
of 10 eccentric contractions with a load corresponding to introducing eccentric resistance exercises, they should
80% MVC strength for nine different muscles) are performed be started from very low-intensity. In this way, eccentric
in a gym. Thus, the results of the present study should be resistance exercises can be safely implemented to novice
considered as an exaggerated case. However, it should be exercisers. Since muscle damage can be easily minimized
noted that if low-intensity eccentric exercise was performed by preconditioning exercise, the use of eccentric resistance
at 2 days prior higher-intensity eccentric exercise, the risk exercises should not be discouraged, and eccentric resistance
was significantly reduced. Actually, it is a general practice exercises should be performed more in a gym, because of
that high-intensity eccentric contractions are performed many positive effects that eccentric resistance training pro-
after several sessions of training consisting of lower-inten- vides (Paschalis et al. 2011; Chen et al. 2017a, b). However,
sity eccentric contractions. Thus, if the training principal of it is not realistic to perform 5 sets of 10 eccentric contrac-
progression is followed, severe muscle damage resulting in tions for several muscles in a session as done in the present
rhabdomyolysis is avoided. study. Performing 2–3 sets of whole body eccentric exercises

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European Journal of Applied Physiology

once or twice a week is possible, which can be completed Data availability The data of the current study are available from the
in 60 min. Further studies are necessary to investigate the corresponding author on reasonable request.
effects of whole body eccentric exercise on health, fitness
and quality of life. Compliance with ethical standards
There are some limitations in the present study. Firstly,
Conflict of interest The authors declare that they have no conflict of
the present study used only young men as participants. It is interest.
necessary to investigate whether the findings of the present
study are applicable for children, women, older individu- Ethical approval All procedures performed in the present study were
als, and clinical populations. Secondly, the interval between in accordance with the ethical standards of the institutional research
committee and with the 1964 Helsinki declaration.
10% EC and 80% EC was 2 days in the current study. Previ-
ous studies showed that the protective effect conferred by Informed consent A written informed consent was obtained from each
10% EC lasted for 2 weeks for the elbow flexors (Chen et al. participant participated in the study.
2012), and 1 week for the knee flexors and knee extensors
(Line et al. 2015). Thus, it is important to examine how
long the protective effect would last for the other muscles
including those investigated in the present study. Thirdly, in References
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