Eur J Appl Physiol

DOI 10.1007/s00421-012-2511-9

ORIGINAL ARTICLE

Comparison of muscle hypertrophy following 6-month

of continuous and periodic strength training
Riki Ogasawara • Tomohiro Yasuda •

Naokata Ishii • Takashi Abe

Received: 18 June 2012 / Accepted: 24 September 2012

Ó Springer-Verlag Berlin Heidelberg 2012

Abstract To compare the effects of a periodic resistance after that. In the PTR group, increase in muscle CSA and
training (PTR) program with those of a continuous resis- strength during the first 3-week detraining/6-week retrain-
tance training (CTR) program on muscle size and function, ing cycle were similar to that in the CTR group during the
14 young men were randomly divided into a CTR group corresponding period. However, increase in muscle CSA
and a PTR group. Both groups performed high-intensity and strength during the second 3-week detraining/6-week
bench press exercise training [75 % of one repetition retraining cycle were significantly higher in the PTR group
maximum (1-RM); 3 sets of 10 reps] for 3 days per week. than in the CTR group. Thus, overall improvements in
The CTR group trained continuously over a 24-week per- muscle CSA and strength were similar between the groups.
iod, whereas the PTR group performed three cycles of The results indicate that 3-week detraining/6-week
6-week training (or retraining), with 3-week detraining retraining cycles result in muscle hypertrophy similar to
periods between training cycles. After an initial 6 weeks of that occurring with continuous resistance training after
training, increases in cross-sectional area (CSA) of the 24 weeks.
triceps brachii and pectoralis major muscles and maximum
isometric voluntary contraction of the elbow extensors and Keywords Muscle hypertrophy
Frequency of training

1-RM were similar between the two groups. In the CTR Resistance training
Detraining
Retraining
group, muscle CSA and strength gradually increased dur-
ing the initial 6 weeks of training. However, the rate of
increase in muscle CSA and 1-RM decreased gradually Introduction

The American College of Sports Medicine and the Amer-

Communicated by Martin Flueck.
ican Geriatrics Society recommend that to achieve muscle
hypertrophy and increased strength, the frequency of pro-
R. Ogasawara
N. Ishii
T. Abe gressive resistance training should be 2–3 days (sessions)
Graduate School of Frontier Sciences, per week (ACSM 1998, 2009; AGS 2001; Garber et al.
University of Tokyo, Kashiwa, Chiba, Japan
2011). It is believed that the acquired training effects may
R. Ogasawara (&) be maintained by as little as a single session per week of
Faculty of Sport and Health Science, Ritsumeikan University, high-intensity exercise (Trappe et al. 2002), while anything
1-1-1 Nojihigashi, Kusatsu, Shiga 525-8577, Japan below this weekly training session will not maintain the
e-mail: [email protected]
acquired muscle adaptations. Thus, exercise must be con-
T. Yasuda tinued on a regular basis, at least once a week, to maintain
Graduate School of Medicine, the effects of training.
University of Tokyo, Tokyo, Japan It is known that the muscle adaptations resulting from
resistance training are less likely to increase after several
T. Abe
Department of Health, Exercise Science and Recreation months of continuous training compared with those
Management, University of Mississippi, Mississippi, USA achieved during the early phase (\3 months) of training. A

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review of previous resistance training studies indicated that body mass 65 ± 10 kg). All subjects were examined by a
the relative increase in the cross-sectional area (CSA) of physician, and none had any medical problems that would
the thigh and upper arm muscles following approximately confound the data from these experiments. They were con-
3 months of training (mainly 2–3 sessions per week) was, sidered to be untrained and had not participated in any regular
on an average, 0.11 and 0.20 % per day, respectively resistance exercise program for at least 2 years prior to the
(Wernbom et al. 2007). After relatively long-term start of this study. Before participating in the study, the sub-
(5–6 months) resistance training, however, the average jects were informed of the methods, procedures, and risks,
increase in thigh muscle CSA was about 0.05 % per day following which they signed an informed consent document.
(Bemben et al. 2000; Hakkinen et al. 1998, 2000, 2003; The study was conducted according to the Declaration of
Hulmi et al. 2009; Narici et al. 1996). Therefore, the rel- Helsinki and was approved by the Ethics Committee for
ative increase in muscle CSA after 5–6 months of training Human Experiments of the University of Tokyo, Japan. The
is probably half that during the early phase of training. subjects were randomly divided into either a continuous
Interestingly, after short-term (\1 month) cessation of resistance training group (CTR, n = 7) or a periodic resis-
training (detraining), muscle adaptation responses may tance training group (PTR, n = 7).
return to their initial levels, and the effects of retraining
after short-term cessation on muscle growth are compara-
Resistance training protocol
ble with those observed during the early phase of training
(Ogasawara et al. 2011). During short-term detraining, the
Both groups performed high-intensity, free-weight bench
rate of decrease (percent change per day) in muscle CSA is
press exercise training 3 days per week. The CTR group
similar to (Andersen et al. 2005; Narici et al. 1989) or even
trained continuously over a 24-week period, while the PTR
less than (Leger et al. 2006; Ogasawara et al. 2011) the
group performed 2 cycles of a 3-week detraining/6-week
increase in muscle CSA during the early phase of training.
retraining period after a 6-week initial training period.
Thus, if the detraining period is followed by a longer
Training intensity was set at 75 % of one repetition (rep)
period of retraining, and if the retraining phase has an
maximum (1-RM), and training volume was set at 3 sets of
effect similar to that of the early phase of training, then
10 reps (with 2–3 min rest between sets). To ensure an
muscle CSA may improve. For example, assuming that the
adequate training load, all training sessions were overseen
decrease in thigh muscle CSA during 3 weeks of detraining
by a supervisor. Training load was renewed every 3 weeks,
is 2.1 % (estimated at 0.10 % per day and 21 days) (Narici
and, if subjects could perform 12 reps or more at the 3rd set
et al. 1989), and the increase in muscle CSA during
during training sessions, the training load was increased by
6 weeks of retraining is 5.9 % (estimated at 0.14 % per day
about 5 % for the next training session. During the
and 42 days) (Narici et al. 1989), the increase in muscle
detraining period, subjects in the PTR group maintained
CSA during a 3-week detraining/6-week retraining period
their normal activities.
(estimated at 0.06 % per day during 9 weeks) would be
3.8 %. The estimated value of 0.06 % per day is similar to
values obtained in previous studies, where the average 1-RM strength tests
increase in thigh muscle CSA was reportedly around
0.05 % per day (Bemben et al. 2000; Hakkinen et al. 1998, Two to 3 weeks before study initiation, all subjects com-
2000, 2003; Hulmi et al. 2009; Narici et al. 1996). pleted two familiarization sessions with submaximum
Therefore, we hypothesized that a 3-week detraining/6- loads (*50 % of predicted 1-RM), where they received
week retraining cycle could produce training effects similar instructions on proper lifting technique. As a warm-up
to those produced by a relatively long and continuous 1 week before the study, the subjects performed 5–6 uni-
resistance training program (5–6 months). The present lateral bench press exercises with a low load (*30–40 %
study aimed to compare the effects of a periodic resistance of predicted 1-RM). After warming up, the load was set at
training program with those of a continuous resistance *80 % of the predicted 1-RM. Following each successful
training program on muscle size and function. lift, the load was increased by *5 % until the subject
failed to lift the load through his entire range of motion. A
test was considered valid if the subject used proper form
Methods and completed the entire lift in a controlled manner without
assistance. On an average, six trials were required to
Subjects complete a 1-RM test (3–5 min rest between each attempt).
1-RM was also assessed every 3 weeks during training for
Fourteen healthy young men volunteered to participate in this each subject. During training sessions as well as 1-RM
study (age 25 ± 3 years, standing height 1.72 ± 0.06 m, testing, the grip width was set at 200 % of the biacromial

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breadth. The coefficient of variation (CV) for these mea- Rate of force development
surements from tests to retests was 1.7 %.
The maximum rate of force development (RFD) was cal-
Measurement of maximum voluntary isometric culated during the MVC trials. RFD was equal to the
contraction (MVC) of the elbow extensors steepest slope calculated for a 20-ms interval, and the
maximum value was used. The CV for these measurements
MVC of the elbow extensors was determined using an is- from tests to retests was 4.6 %.
okinetic dynamometer (Biodex System 3, Biodex Medical
Systems Inc., Shirley, NY, USA). A subject sat comfort-
Muscle size measurements
ably on a chair, with the arm positioned on a firm and
stable table at chest level and an elbow joint angle of 90°
Multi-slice magnetic resonance imaging (MRI) of the
(0° at full extension). The upper arm was maintained in the
upper arm and chest was performed using a General
horizontal plane (at 90°), while the subject’s wrist was
Electric Yokogawa Signa 0.2-T scanner (Milwaukee, WI,
fixed at the end of the lever arm in a position halfway
USA). A T1-weighted, spin-echo, axial plane sequence was
between supination and pronation. The elbow extension
generated with a 520-ms repetition time and a 20-ms echo
torque was measured with a transducer, while a diagonal
time. The subject rested quietly in the magnet bore in a
strap was secured over the elbow to maintain a stationary
supine position with his arms extended. The lateral epi-
position during MVC. Each subject was instructed to
condyle of the humerus was used as the point of origin, and
contract as rapidly and as forcefully as possible. MVC was
continuous transverse images of 1.0-cm slice thickness
measured three times, and the maximum value was used. A
were obtained from the lateral epicondyle of the humerus
1-min rest was allowed between trials to eliminate the
to the acromial process of the scapula. All MRI data were
effects of fatigue. The MVC test was performed before and
transferred to a personal computer for analysis using spe-
every 3 weeks during the study. The CV for these mea-
cially designed image analysis software (TomoVision Inc.,
surements from tests to retests was 3.1 %.
Montreal, Canada). For each slice, skeletal muscle CSA
was digitized, and the muscle tissue volume (cm3) per slice
Electromyography (EMG) measurements
was calculated by multiplying muscle tissue area (cm2)
with slice thickness (cm). The CSA at 25, 50, and 75 %
EMG activity during MVC of elbow extensors was recor-
from the lateral epicondyle of the humerus to the acromial
ded. The skin was shaved, abraded with a skin preparation
process of the scapula and the belly of the TB (TB-CSA)
gel (Skinpure, Nihon Kohden, Japan), and cleaned with
and pectoralis major (PM; PM-CSA) muscles was deter-
alcohol wipes. During all experiments, skin impedance was
mined for three continuous slices using the same slice
\2 kX. The ground electrode was positioned on the lateral
number from the point of origin. These were averaged for
epicondyle. Bipolar electrodes (Vitrode F, Ag/AgCl, 1-cm
statistical analysis. Muscle volume of the individual muscle
diameter, Nihon Kohden, Tokyo, Japan) were placed over
was defined as the summation of the slices of muscle.
the belly of the muscle with a constant interelectrode dis-
These measurements were performed before the study and
tance of 20 mm. The electrodes were connected to a pre-
after the training/retraining (weeks 6, 15, and 24) and
amplifier of a differential amplifier having a bandwidth of
detraining (weeks 9 and 18) periods in the PTR group.
0 Hz–500 kHz (AB 6216, Nihon Kohden, Tokyo, Japan).
Measurements for the CTR group were performed at the
EMG signals were collected continuously from the triceps
same time points as those for the PTR group. The CV for
brachii (TB; an agonist muscle) and the biceps brachii (BB;
these measurements was \1 %.
an antagonist muscle) muscles at a sampling rate of
1,024 Hz using a 12-bit analog-to-digital converter (Mac-
intosh, Power PC 750, Apple, Japan). To determine inte- Statistical analysis
grated EMG activity (iEMG), signals were fully rectified
and integrated (Power Lab Chart 5 software, ADInstru- Results are expressed as mean and standard deviations
ments, Japan). iEMG in the BB muscle was normalized as (SD). Changes in CSA, 1-RM, MVC, agonist and antago-
a percentage of the maximum isometric value of the nist iEMG, RFD, and RFD/MVC were compared by two-
muscle when it was acting as an agonist, and this value was way ANOVA with repeated measures (group 9 time). Post
used to calculate the level of antagonist coactivation during hoc analyses used t tests with the Benjamini and Hochberg
elbow extension. EMG activity was quantified over a per- False Discovery Rate correction for multiple comparisons.
iod of 1,000 ms around the peak torque of each contrac- All baseline characteristics and relative changes over the
tion. The CV for these measurements from tests to retests 24-week period were compared between groups by Stu-
was 1.9 %. dent’s t test. The magnitude of changes in muscle size and

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strength was also compared between the detraining and TB-CSA, and PM-CSA were similar between the two
retraining periods by one-way ANOVA. Significance was groups (Fig. 1). The rate of increase in TB-CSA and PM-
set at P \ 0.05. All analyses were performed using JMP CSA was similar, i.e., approximately 0.23 and 0.39 % per
statistical software, version 8.0 (SAS Institute, Cary, NC, day, respectively, between both groups (Fig. 2).
USA).
Effects of training in the CTR group

Results MVC, dynamic 1-RM strength, TB-CSA, and PM-CSA

gradually increased after the initial 6 weeks of training
Baseline characteristics (Fig. 1). However, the rate of increase in muscle CSA and
dynamic strength gradually declined with time throughout
At baseline, there were no significant differences in age the training period; the rate during the initial 0–6 weeks
and anthropometric variables between the CTR and PTR was significantly greater than that during weeks 9–15,
groups. MVC, dynamic 1-RM strength, and muscle CSA weeks 15–18, and weeks 18–24 (Fig. 2). After the 24-week
and volume of TB and PM muscle were also similar training period, the rate of average increase in TB-CSA and
between the two groups (Table 1). PM-CSA was 0.13 and 0.22 % per day, respectively. The
rate of increase in MVC tended to be greater during the
Effects of initial 6-week training in both groups initial 0–6 weeks compared with that during weeks 6–9,
although these rates were not significantly different
There was no difference in training volume (load 9 reps) (Fig. 2). Although RFD and agonist iEMG gradually
after initial 6 weeks of training between groups (CTR increased with training (time effect P \ 0.05), there were
20,385 kg, PTR 19,417 kg). After the initial 6 weeks of no significant changes in RFD and agonist iEMG between
training, the increase in muscle strength (1-RM and MVC), each training period (Figs. 3, 4).

Table 1 Descriptive characteristics and effects of 24 weeks of training on maximal strength (1-RM and MVC) and muscle size (muscle CSA
and volume)
CTR (n = 7) PTR (n = 7)
Pre Post Change (%) Pre Post Change (%)

Age (years) 25.1 ± 3.2 24.3 ± 1.9

Height (cm) 173 ± 8 170 ± 3
Body mass (kg) 65.4 ± 6.2 66.6 ± 7.2* 65.1 ± 12.8 66.5 ± 13.2*
*
1-RM (kg) 51.1 ± 9.9 77.4 ± 16.9 51.3 47.1 ± 10.6 70.4 ± 13.6* 50.0
*
MVC (Nm) 30.8 ± 6.7 39.2 ± 6.7 28.7 30.0 ± 6.4 38.9 ± 6.8* 31.3
Muscle CSA (cm2)
TB
Belly 22.2 ± 4.3 26.6 ± 3.9* 21.0 20.2 ± 2.3 24.1 ± 2.4* 19.3
*
25 % 14.3 ± 2.5 17.0 ± 2.9 19.5 13.0 ± 3.5 15.4 ± 3.1* 20.0
50 % 21.5 ± 3.5 25.8 ± 2.8* 20.9 19.4 ± 2.5 23.2 ± 2.7* 19.7
75 % 19.8 ± 5.3 23.5 ± 5.5* 19.8 16.2 ± 1.7 19.5 ± 2.0* 18.9
PM
Belly 29.7 ± 6.4 40.6 ± 8.7* 36.9 26.3 ± 4.8 35.5 ± 7.3* 35.0
*
25 % 15.2 ± 5.7 20.7 ± 7.7 36.3 15.7 ± 3.9 21.1 ± 15.5* 34.3
50 % 27.7 ± 5.8 38.0 ± 8.3* 37.3 26.8 ± 5.6 36.6 ± 8.8* 36.2
75 % 25.2 ± 3.4 35.1 ± 3.1* 40.0 24.0 ± 4.0 32.9 ± 6.3* 37.3
Muscle volume (cm3)
TB 263 ± 65 316 ± 70* 21.4 246 ± 31 293 ± 33* 19.6
*
PM 276 ± 66 383 ± 96 39.4 253 ± 51 346 ± 78* 36.1
Values are mean ± SD
CTR continuous training group, PTR periodic training group, CSA cross-sectional area, 1-RM one repetition maximum, MVC maximal voluntary
isometric contraction, TB triceps brachii, PM pectoralis major
* P \ 0.05 versus Pre

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Fig. 1 Time course of changes A B

in cross-sectional area (CSA) of
a the triceps brachii (TB)
muscle (TB-CSA) and b the
pectoralis major (PM) muscle
(PM-CSA), c one-repetition
maximal (1-RM) strength, and
d maximum voluntary isometric
contraction (MVC) of the elbow
extensors *Significantly
different from that in the
periodic training group;
P \ 0.05. CTR continuous
training group, PTR periodic C D
training group

Fig. 2 Rate of change in a the A B

cross-sectional area (CSA) of
the triceps brachii (TB) muscle
(TB-CSA), b CSA of the
pectoralis major (PM) muscle
(PM-CSA), c one-repetition
maximal (1-RM) strength and
maximum voluntary isometric
contraction (MVC) of the elbow
extensors, and d maximum
strength during periodic
resistance training (PTR) and
continuous resistance training
(CTR). *Significantly different C D
from that during weeks 0–6;
P \ 0.05

Effects of training in the PTR group differences in the increase in TB-CSA between the initial
6-week training period and the first and second 6-week
During the first (weeks 6–9) and second (weeks 15–18) retraining periods (Fig. 2). Therefore, during the first and
3-week detraining periods, the decrease in TB-CSA was second 3-week detraining/6-week retraining cycles, TB-
2.6 % (0.14 % per day) and 2.9 % (0.16 % per day), CSA increased by 5.0 and 4.6 %, respectively. The rate of
respectively. In contrast, the increase in TB-CSA during average increase in TB-CSA was 0.11 % per day after the
the first (weeks 9–15) and second (weeks 18–24) 6-week 24-week experimental period. Similar results were
retraining periods was 7.6 % (0.20 % per day) and 7.5 % observed for the PM muscle; the rate of average increase in
(0.20 % per day), respectively. There were no significant PM-CSA was 0.21 % per day after the 24-week period.

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Fig. 3 Time course of changes

in a relative one-repetition
A 40 B
CTR 20 CTR

1-RM / TB-CSA (% change)

VC/TB-CSA (% change)
maximal (1-RM) strength/cross- PTR PTR
sectional area (CSA) of the 15
30
triceps brachii (TB) muscle (TB- 10
CSA), b relative maximum 20 5
voluntary isometric contraction
(MVC) of the elbow extensors/ 0
10
TB-CSA, c rate of force -5
5

MV
development (RFD), d RFD/
MVC, and e integrated 0 -10
0 3 6 9 12 15 18 21 24 0 3 6 9 12 15 18 21 24
electromyographic activity
(iEMG) of the agonist and Training weeks Training weeks
f antagonist muscles. CTR
continuous training group, PTR C 80 CTR D 40 CTR
periodic training group PTR PTR

R FD/MVC (% change)
30
60
RFD (% change)

20
40 10

20 0
-10
0
-20
-20 -30
0 3 6 9 12 15 18 21 24 0 3 6 9 12 15 18 21 24
Training weeks Training weeks

E F
120 CTR 80 CTR

nge)
Agonist iEMG (% change)

PTR PTR
60

Anttagonist iEMG (% chan

90
60 40
20
30
0
0
-20
-30 -40
-60 -60
0 3 6 9 12 15 18 21 24 0 3 6 9 12 15 18 21 24
Training weeks Training weeks

Dynamic 1-RM strength decreased slightly (-2.0 % muscle CSA in TB and PM muscle (Table 1). In the PTR
during the first and -3.3 % during the second), whereas group, which included a total of 6 weeks of detraining, there
MVC remained unchanged during the first and second were 25 % fewer total training sessions and 33.5 % fewer
3-week detraining periods (Fig. 2). During the first and total training volume (CTR 96,942 kg, PTR 64,509 kg)
second 6-week retraining periods, 1-RM strength increased throughout the 24-week training period. We calculated the
by 15.3 and 12.7 %, respectively, whereas MVC increased rate of increase in muscle CSA and strength per session
by 6.7 and 7.3 %, respectively. The increase in 1-RM (Fig. 5). During the first 3-week detraining/6-week retrain-
strength and MVC was comparable between the initial ing cycle (weeks 6–15), increase in CSA of the TB and PM
6-week training period and the first and second 6-week muscles and strength was similar between the CTR and PTR
retraining periods (Fig. 2). Overall, RFD and agonist iEMG groups. However, this increase was significantly higher
increased with PTR program (time effect P \ 0.05) (Fig. 3). during the second 3-week detraining/6-week retraining cycle
However, there were no significant changes in those during in the PTR group than that during the corresponding period in
each detraining and retraining period (Figs. 3, 4). the CTR group, with the exception of MVC.

Comparisons between the CTR and PTR groups

Discussion
After 24 weeks, the total improvement in muscle CSA and
volume of TB and PM and maximum strength (1-RM and For this study, we hypothesized that the total improvement
MVC) were similar between the two training groups in muscle CSA would be similar between a continuous
(Table 1). There were no significant regional differences in resistance group (24 continuous weeks of resistance

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Fig. 4 Rate of change in A B

a relative one-repetition
maximal (1-RM) strength/cross-
sectional area (CSA) of the
triceps brachii (TB) muscle (TB-
CSA), b relative maximum
voluntary isometric contraction
(MVC)/TB-CSA, c rate of force
development (RFD), d RFD/
MVC, and e integrated
electromyographic activity
(iEMG) of the agonist and
f antagonist muscles during
periodic resistance training C D
(PTR) and continuous resistance
training (CTR). *Significantly
different from that during weeks
0–6; P \ 0.05

E F

training) and a periodic resistance group (three 6-week It is known that muscle adaptations are less likely to
training cycles with two 3-week detraining periods increase after several months of continuous training com-
between cycles). The key elements of our hypothesis were pared with the increase during the early phase of training.
whether the muscle adaptation responses would return to However, there are very few published long-term studies
their initial levels after short-term training cessation, and on this issue. In this study, we observed that the increase in
whether the effects of retraining on muscle growth after TB-CSA was 0.25 % per day during the initial 6 weeks of
short-term cessation would be comparable to those on training and 0.13 % per day during the total 24 weeks of
muscle growth during the initial phase of training. Our training; the latter value was approximately half the former
results showed that, in the PTR group, the increase in value. In particular, the increase in muscle CSA was less
muscle CSA and 1-RM strength was similar between the than 0.10 % per day after 9 weeks of training. Therefore, if
initial 6-week training period and the first and second the rate of decrease in muscle CSA is similar between
6-week retraining periods. In contrast, the rate of increase detraining and retraining, a twofold longer period of
in muscle CSA and 1-RM strength gradually decreased retraining may provide equivalent improvements in muscle
with time throughout the 24 weeks of training in the CTR CSA when compared with continuous long-term training.
group. As a result, the increase in TB-CSA, PM-CSA, We found that the rate of change in TB-CSA was
MVC of the elbow extensors, and 1-RM bench press -0.16 % per day during the 3 weeks of detraining and
strength were similar between the CTR and PTR groups, 0.19 % per day during the 6 weeks of retraining. Our
even though the PTR group had 25 % fewer training ses- results suggest that training-induced muscle adaptations
sions compared with the CTR group. may recover to the levels observed during the initial phases

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Fig. 5 Potential for increase in

hypertrophy and strength (%
A B
increase per session) for a cross-
sectional area (CSA) of the
triceps brachii (TB) muscle (TB-
CSA) and b the pectoralis major
(PM) muscle (PM-CSA), c one-
repetition maximal (1-RM)
strength, and d maximum
voluntary isometric contraction
(MVC) of the elbow extensors
during periodic resistance
training (PTR filled square) and
continuous resistance training
(CTR open square).
*Significantly different from
C D
that in the CTR group; P \ 0.05

of training when individuals are subjected to a 3-week sensitive again after a short detraining or non-training
detraining period. Therefore, 3-week detraining/6-week period. These mechanisms may be responsible for
retraining cycles for 24 weeks may induce hypertrophic retraining-induced muscle hypertrophy and the advantage
responses similar to those induced by continuous training of periodic training programs, at least in young individuals.
cycles for 24 weeks. Interestingly, our PTR group exhib- Future studies should address the cellular and molecular
ited an identical increase in TB-CSA and PM-CSA muscles mechanisms underlying the changes in sensitivity of the
during the second retraining period (weeks 18–24). If the muscle to the training stimulus.
same retraining effects occurred after 24 weeks of training, Although it is currently unclear whether satellite cells are
and if continuous long-term training induced decreased necessary for muscle hypertrophy, we know that these cells
muscle adaptations, 3-week detraining/6-week retraining definitely play an indispensable role in the muscle regener-
cycles may produce greater muscle hypertrophic responses ation process (McCarthy et al. 2011; Pallafacchina et al.
compared with continuous training cycles after 24 weeks. 2012; Relaix and Zammit 2012). Since strenuous exercise is
Our results are in agreement with those of the previous considered to cause microtrauma to muscle fibers, satellite
cellular and molecular studies. Chronic muscle contraction cells may be essential especially during the initial phase of
induces a variety of metabolic and morphological adapta- training or reuptake of exercise for inducing potent hyper-
tions in contracted skeletal muscles for maintaining trophy. Some previous studies have reported that regenera-
homeostasis and minimizing cellular disturbances during tive capacity reduces with age, because of reduced satellite
subsequent training sessions (Gordon et al. 2012; Hubal cell activation or content (Castets et al. 2011; Day et al. 2010;
et al. 2008). In the muscle, anabolic mammalian target of Renault et al. 2002). Compared to the young individuals, the
rapamycin (mTOR) signaling and protein synthesis older individuals showed an attenuated rate and magnitude
responses to resistance exercise are attenuated by chronic of increase in muscle mass after 4 weeks of retraining fol-
resistance training (Coffey et al. 2006; Phillips et al. 1999, lowing 2 weeks of immobilization (Suetta et al. 2009). Thus,
2002; Tang et al. 2008). These results may explain the it is possible that older individuals display an attenuated
attenuated muscle hypertrophy response observed during muscle hypertrophic response to retraining following
the late phase compared to the early phase of resistance detraining as well as immobilization. Additional studies are
training. In contrast, our results suggest that although needed for the clinical application of periodic resistance
greater relative stimulation (i.e., greater intensity, volume, training in older individuals.
frequency) would be required to sustain anabolic responses A previous study by Kawakami et al. (1995) found that
for further adaptations, these responses would become TB-CSA increased by 31.7 % (0.28 % per day) after

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16 weeks of high-intensity (80 % of 1-RM, 3 days a the initial 6-week training period and the first and second
week), unilateral elbow extension (French press) exercise retraining periods in the PTR group. There were also no
training. Kraemer et al. (2004) reported an increase of significant changes in agonist and antagonist iEMG activities
17.9 % (0.11 % per day) in TB-CSA after 24 weeks of during the retraining periods. A previous study observed that
high-intensity (3–8 RM), upper body (e.g., bench press, EMG activity was not significantly changed during
triceps pushdown) resistance training. Our results were 12 weeks of retraining after 24 weeks of detraining (Ha-
similar to those of this study (Kraemer et al. 2004) in that kkinen et al. 2003). Therefore, it would appear that increased
the rate of increase in TB-CSA was 0.13 % per day during muscle CSA may contribute primarily to improving muscle
the 24 weeks of bench press training. By comparison, the strength during retraining.
percent increase in PM-CSA was greater than that in TB- Previous studies reported that an increase in twitch RFD
CSA after 24 weeks of training. Till date, very few studies was observed after 8 weeks or 3 months of detraining
have reported hypertrophy in muscles of the trunk fol- (Andersen et al. 2005; Ishida et al. 1990). This phenomenon
lowing high-intensity resistance training. One study by Abe may be attributed to enhanced muscle excitation–contrac-
et al. (2000) found that the time course of increase in tion coupling and/or the cross-bridge cycling rate resulting
muscle thickness was greater in the chest than in the upper from myosin heavy chain (MHC) transitions to faster-
arm after 12 weeks of total body resistance training. responding isoforms (Andersen et al. 2005). In the present
Because chest muscles are probably untrained compared study, however, RFD did not change significantly during
with the arm muscles, especially in previously untrained the 3 weeks of detraining or the 6 weeks of retraining. The
subjects, the relative increase in chest muscle size may be difference between previous studies (Andersen et al. 2005;
greater than that in upper arm muscle size. Ishida et al. 1990) and the present study is the duration of
It is clear that the magnitude of the decline in muscle size is the detraining period; our 3 weeks of detraining may have
associated with the duration of detraining, although the rate of been insufficient to cause a shift in MHC isoforms and alter
decline is not constant. Our results showed that a decrease in RFD independent of MVC changes.
TB-CSA was 2.6 % (0.14 % per day) and 2.9 % (0.16 % per The American College of Sports Medicine (ACSM) and
day) during the first and second 3-week detraining periods, other international organizations have established guide-
respectively. Andersen et al. (2005) reported a significant lines for resistance training. In general, it is recommended
increase in CSA of the quadriceps muscle after 3 months of that a loading range of more than 65 % of 1-RM be used
resistance training; however, it decreased to the pretraining for 8–12 repetitions per set for three sets per exercise for
level after 3 months of detraining. Leger et al. (2006) 2–3 days per week (ACSM 2009; Baechle and Earle 2008;
investigated muscle adaptations after 8 weeks of both Bird et al. 2005; Kraemer and Ratamess 2004). However,
hypertrophy-stimulating resistance training and atrophy- evidence suggests that even recreational weightlifters find
stimulating detraining. They found that half of the training- it difficult to perform these training programs continuously,
induced muscle hypertrophy was still present after 8 weeks of because of various reasons such as reduced motivation or
detraining. Furthermore, Hather et al. (1991) reported that orthopedic injury (Hass et al. 2000). Therefore, reduced
most of the training-induced increase in muscle fiber area was time commitment and exercise volume may decrease
still maintained after 4 weeks of detraining. Therefore, the physical and psychological strain and lead to greater par-
rate of detraining-induced muscle atrophy may be lesser than ticipation in resistance training programs.
that of training-induced muscle hypertrophy. However, the In summary, our results suggest that although improve-
degree of detraining-induced muscle atrophy is complex and ments induced by periodic training do not appear to exceed
currently unclear. those induced by continuous training after a total of
During the first and second 3-week detraining periods, we 24 weeks, a relatively short detraining period does not
found that 1-RM strength decreased slightly (-2.0 and attenuate the muscle adaptations that occur over 24 weeks of
-3.3 %, respectively), while MVC remained unchanged resistance training and is effective intervention to maintain
(0.3 and 0.7 %, respectively). Previous studies have reported muscle adaptation during late phase of resistance training.
no significant decrease in muscle strength after short-term
(2–6 weeks) detraining (Hortobagyi et al. 1993; Kraemer Conflict of interest None declared.
et al. 2002). Recently, one study found no significant change
in the neural activation level after 3 months of detraining
because muscle CSA had decreased to its pretraining level References
(Kubo et al. 2010). Therefore, the relatively short duration of
Abe T, DeHoyos DV, Pollock ML, Garzarella L (2000) Time course
detraining did not affect the increase in training-induced for strength and muscle thickness changes following upper and
muscle strength. In comparison, there were no significant lower body resistance training in men and women. Eur J Appl
differences in the rate of increase in 1-RM and MVC between Physiol 81:174–180

123
 Eur J Appl Physiol

ACSM (1998) American College of Sports Medicine Position Stand. Neuromuscular adaptations during concurrent strength and
The recommended quantity and quality of exercise for develop- endurance training versus strength training. Eur J Appl Physiol
ing and maintaining cardiorespiratory and muscular fitness, and 89:42–52
flexibility in healthy adults. Med Sci Sports Exerc 30:975–991 Hass CJ, Garzarella L, de Hoyos D, Pollock ML (2000) Single versus
ACSM (2009) American College of Sports Medicine position stand. multiple sets in long-term recreational weightlifters. Med Sci
Progression models in resistance training for healthy adults. Med Sports Exerc 32:235–242
Sci Sports Exerc 41:687–708 Hather BM, Tesch PA, Buchanan P, Dudley GA (1991) Influence of
AGS (2001) Exercise prescription for older adults with osteoarthritis eccentric actions on skeletal muscle adaptations to resistance
pain: consensus practice recommendations. A supplement to the training. Acta Physiol Scand 143:177–185
AGS Clinical Practice Guidelines on the management of chronic Hortobagyi T, Houmard JA, Stevenson JR, Fraser DD, Johns RA,
pain in older adults. J Am Geriatr Soc 49:808–823 Israel RG (1993) The effects of detraining on power athletes.
Andersen LL, Andersen JL, Magnusson SP, Suetta C, Madsen JL, Med Sci Sports Exerc 25:929–935
Christensen LR, Aagaard P (2005) Changes in the human muscle Hubal MJ, Chen TC, Thompson PD, Clarkson PM (2008) Inflamma-
force-velocity relationship in response to resistance training and tory gene changes associated with the repeated-bout effect. Am J
subsequent detraining. J Appl Physiol 99:87–94 Physiol Regul Integr Comp Physiol 294:R1628–R1637
Baechle T, Earle R (2008) Essentials of strength training and Hulmi JJ, Kovanen V, Selanne H, Kraemer WJ, Hakkinen K, Mero
conditioning. Human kinetics, Champaign AA (2009) Acute and long-term effects of resistance exercise
Bemben DA, Fetters NL, Bemben MG, Nabavi N, Koh ET (2000) with or without protein ingestion on muscle hypertrophy and
Musculoskeletal responses to high- and low-intensity resistance gene expression. Amino Acids 37:297–308
training in early postmenopausal women. Med Sci Sports Exerc Ishida K, Moritani T, Itoh K (1990) Changes in voluntary and
32:1949–1957 electrically induced contractions during strength training and
Bird SP, Tarpenning KM, Marino FE (2005) Designing resistance detraining. Eur J Appl Physiol Occup Physiol 60:244–248
training programmes to enhance muscular fitness: a review of the Kawakami Y, Abe T, Kuno SY, Fukunaga T (1995) Training-induced
acute programme variables. Sports Med 35:841–851 changes in muscle architecture and specific tension. Eur J Appl
Castets P, Bertrand AT, Beuvin M, Ferry A, Le Grand F, Castets M, Physiol Occup Physiol 72:37–43
Chazot G, Rederstorff M, Krol A, Lescure A, Romero NB, Kraemer WJ, Ratamess NA (2004) Fundamentals of resistance
Guicheney P, Allamand V (2011) Satellite cell loss and impaired training: progression and exercise prescription. Med Sci Sports
muscle regeneration in selenoprotein N deficiency. Hum Mol Exerc 36:674–688
Genet 20:694–704 Kraemer WJ, Nindl BC, Ratamess NA, Gotshalk LA, Volek JS, Fleck
Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR, SJ, Newton RU, Hakkinen K (2004) Changes in muscle
Hawley JA (2006) Early signaling responses to divergent hypertrophy in women with periodized resistance training. Med
exercise stimuli in skeletal muscle from well-trained humans. Sci Sports Exerc 36:697–708
FASEB J 20:190–192 Kubo K, Ikebukuro T, Yata H, Tsunoda N, Kanehisa H (2010) Time
Day K, Shefer G, Shearer A, Yablonka-Reuveni Z (2010) The course of changes in muscle and tendon properties during
depletion of skeletal muscle satellite cells with age is concom- strength training and detraining. J Strength Cond Res 24:322–
itant with reduced capacity of single progenitors to produce 331
reserve progeny. Dev Biol 340:330–343 Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, Crettenand A,
Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Gobelet C, Rohmer P, Konzelmann M, Luthi F, Russell AP
Lee IM, Nieman DC, Swain DP (2011) American College of (2006) Akt signalling through GSK-3beta, mTOR and Foxo1 is
Sports Medicine position stand. Quantity and quality of exercise involved in human skeletal muscle hypertrophy and atrophy.
for developing and maintaining cardiorespiratory, musculoskele- J Physiol 576:923–933
tal, and neuromotor fitness in apparently healthy adults: guidance McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui
for prescribing exercise. Med Sci Sports Exerc 43:1334–1359 AB, Srikuea R, Lawson BA, Grimes B, Keller C, Van Zant G,
Gordon PM, Liu D, Sartor MA, IglayReger HB, Pistilli EE, Gutmann Campbell KS, Esser KA, Dupont-Versteegden EE, Peterson CA
L, Nader GA, Hoffman EP (2012) Resistance exercise training (2011) Effective fiber hypertrophy in satellite cell-depleted
influences skeletal muscle immune activation: a microarray skeletal muscle. Development 138:3657–3666
analysis. J Appl Physiol 112:443–453 Narici MV, Roi GS, Landoni L, Minetti AE, Cerretelli P (1989)
Kraemer WJ, Koziris LP, Ratamess NA, Hakkinen K, TR-M NT, Fry Changes in force, cross-sectional area and neural activation
AC, Gordon SE, Volek JS, French DN, Rubin MR, Gomez AL, during strength training and detraining of the human quadriceps.
Sharman MJ, Michael Lynch J, Izquierdo M, Newton RU, Fleck Eur J Appl Physiol Occup Physiol 59:310–319
SJ (2002) Detraining produces minimal changes in physical Narici MV, Hoppeler H, Kayser B, Landoni L, Claassen H, Gavardi
performance and hormonal variables in recreationally strength- C, Conti M, Cerretelli P (1996) Human quadriceps cross-
trained men. J Strength Cond Res 16:373–382 sectional area, torque and neural activation during 6 months
Hakkinen K, Newton RU, Gordon SE, McCormick M, Volek JS, strength training. Acta Physiol Scand 157:175–186
Nindl BC, Gotshalk LA, Campbell WW, Evans WJ, Hakkinen Ogasawara R, Yasuda T, Sakamaki M, Ozaki H, Abe T (2011) Effects
A, Humphries BJ, Kraemer WJ (1998) Changes in muscle of periodic and continued resistance training on muscle CSA and
morphology, electromyographic activity, and force production strength in previously untrained men. Clin Physiol Funct
characteristics during progressive strength training in young and Imaging 31:399–404
older men. J Gerontol A Biol Sci Med Sci 53:B415–B423 Pallafacchina G, Blaauw B, Schiaffino S (2012) Role of satellite cells
Hakkinen K, Alen M, Kallinen M, Newton RU, Kraemer WJ (2000) in muscle growth and maintenance of muscle mass. Nutr Metab
Neuromuscular adaptation during prolonged strength training, Cardiovasc Dis [Epub ahead of print]
detraining and re-strength-training in middle-aged and elderly Phillips SM, Tipton KD, Ferrando AA, Wolfe RR (1999) Resistance
people. Eur J Appl Physiol 83:51–62 training reduces the acute exercise-induced increase in muscle
Hakkinen K, Alen M, Kraemer WJ, Gorostiaga E, Izquierdo M, protein turnover. Am J Physiol 276:E118–E124
Rusko H, Mikkola J, Hakkinen A, Valkeinen H, Kaarakainen E, Phillips SM, Parise G, Roy BD, Tipton KD, Wolfe RR, Tamopolsky
Romu S, Erola V, Ahtiainen J, Paavolainen L (2003) MA (2002) Resistance-training-induced adaptations in skeletal

123
Eur J Appl Physiol

muscle protein turnover in the fed state. Can J Physiol Pharmacol Tang JE, Perco JG, Moore DR, Wilkinson SB, Phillips SM (2008)
80:1045–1053 Resistance training alters the response of fed state mixed muscle
Relaix F, Zammit PS (2012) Satellite cells are essential for skeletal protein synthesis in young men. Am J Physiol Regul Integr
muscle regeneration: the cell on the edge returns centre stage. Comp Physiol 294:R172–R178
Development 139:2845–2856 Trappe S, Williamson D, Godard M (2002) Maintenance of whole
Renault V, Thornell LE, Eriksson PO, Butler-Browne G, Mouly V muscle strength and size following resistance training in older
(2002) Regenerative potential of human skeletal muscle during men. J Gerontol A Biol Sci Med Sci 57:B138–B143
aging. Aging Cell 1:132–139 Wernbom M, Augustsson J, Thomee R (2007) The influence of
Suetta C, Hvid LG, Justesen L, Christensen U, Neergaard K, frequency, intensity, volume and mode of strength training on
Simonsen L, Ortenblad N, Magnusson SP, Kjaer M, Aagaard P whole muscle cross-sectional area in humans. Sports Med
(2009) Effects of aging on human skeletal muscle after 37:225–264
immobilization and retraining. J Appl Physiol 107:1172–1180

123