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8/6/2019 MSSE 2005 GOTO - The Impaact of Metabolic Stress on Hormonal Responses and Muscular Adaptations
The Impact of Metabolic Stress on HormonalResponses and Muscular Adaptations
KAZUSHIGE GOTO1, NAOKATA ISHII2, TOMOHIRO KIZUKA1, and KAORU TAKAMATSU1
1 Institute of Health and Sport Sciences, University of Tsukuba, Tsukuba, Ibaraki, JAPAN; and 2 Department of LifeSciences, Graduate School of Arts and Sciences, University of Tokyo, Komaba, Tokyo, JAPAN
ABSTRACT
GOTO, K., N. ISHII, T. KIZUKA, and K. TAKAMATSU. The Impact of Metabolic Stress on Hormonal Responses and Muscular
Adaptations. Med. Sci. Sports Exerc., Vol. 37, No. 6, pp. 955–963, 2005. Purpose: The purpose of this study was to examine the impact
of exercise-induced metabolic stress on hormonal responses and chronic muscular adaptations. Methods: We compared the acute and
long-term effects of an “NR regimen” (no-rest regimen) and those of a “WR regimen” (regimen with rest period within a set).
Twenty-six male subjects were assigned to either the NR ( N 9), WR ( N 9), or control (CON, N 8) groups. The NR regimen
consisted of 3–5 sets of 10 repetitions at 10-repetition maximum (RM) with an interset rest period of 1 min (lat pulldown, shoulder
press, and bilateral knee extension). In the WR regimen, subjects completed the same protocol as the NR regimen, but took a 30-s rest
period at the midpoint of each set of exercises in order to reduce exercise-induced metabolic stress. Acute hormonal responses to both
regimens were measured followed by a 12-wk period of resistance training. Results: Measurements of blood lactate and serum hormoneconcentrations after the NR and WR regimens showed that the NR regimen induced strong lactate, growth hormone (GH), epinephrine
(E), and norepinephrine (NE) responses, whereas the WR regimen did not. Both regimens failed to cause significant changes in
testosterone. After 12 wk of resistance training, the NR regimen caused greater increases in 1RM (P 0.01), maximal isometric
strength (P 0.05), and muscular endurance (P 0.05) with knee extension than the WR regimen. The NR group showed a marked
increase (P 0.01) in muscle cross-sectional area, whereas the WR and CON groups did not. Conclusion: These results suggest that
exercise-induced metabolic stress is associated with acute GH, E, and NE responses and chronic muscular adaptations following
Values are means SE. Pre and post indicate the values obtained before and after thetraining period, respectively. * Significant difference from pretraining value (P 0.05);** significant difference from pretraining value (P 0.01).
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acquired with the field of view, repetition time, and echo
time being 240 mm, 800 ms, and 20 ms, respectively, and
the scan matrix 256 256. Image acquisition was started
after the subject lied in the supine position with his legs
extended and relaxed. The scan time was approximately
13–15 min.
From the obtained serial sections, those for two portions
near the midpoint (halfway between the trochanter major
and head of the tibia) of the thigh were chosen for the
analysis of muscle CSA. On the selected cross-sectional
images, the outlines of quadriceps femoris (QF) were traced
by the same expert. Traced images were inputted into a
computer (Power Macintosh G4, Apple Computer), and the
CSA of the QF were measured using NIH image software
(version 1.61). The maximal isometric strength per unit of
CSA was then determined as an index of neuromuscular
function. The measurements were repeated twice for each
image, and the mean values were adopted. A strong corre-
lation between the first and second measurements (r 0.99)
indicated a high reliability of the measurements.
Statistical analysis. Data are expressed as means
SE. In the study on acute hormonal response to the NR and
WR regimens, a two-way analysis of variance (ANOVA)
with repeated measures was used. In the event of a signif-
icant F -ratio, a Tukey’s HSD post hoc test was used to
compare means. In the study on the long-term effects of
resistance training, a two-way ANOVA with repeated mea-
sures and a Tukey’s HSD post hoc were used. Differences
between the percent changes among the three (NR, WR,
CON) groups were examined by a one-way ANOVA fol-
lowed by a Tukey’s HSD post hoc test. A selective bivariate
relationship was investigated using a Pearson product–mo-
ment correlation coefficient. P 0.05 was considered as
significant.
RESULTS
Acute hormonal and lactate responses. Figures 1
and 2 show acute changes in blood LA, serum GH, and TES
(Fig. 1), and plasma E and NE (Fig. 2) before the period of
training. No significant difference was seen in resting LA
and hormone concentrations between the exercise regimens.
In the NR regimen, LA and hormone concentrations (except
for that of TES) showed significant elevations after exercise,
whereas those of the WR regimen showed no significantchanges except for LA and NE. Between the NR and WR
regimens, significant differences were observed in the post-
exercise concentrations of LA, GH, and NE, among which
GH showed the largest difference. When the GH response was
assessed by the area under the time-concentration relation-
ship (GHauc), the value after the NR regimen (559.6
200.9 ngmL1) was approximately threefold higher than that
after the WR regimen (185.0 86.7 ngmL1; P 0.05).
However, no significant difference was seen in TES concen-
trations between the two regimens, although the postexercise
value (30 min) in the NR regimen was lower than its preex-
ercise value (P 0.05).
Changes in muscle cross-sectional area and
body composition. Changes in physical characteristics
over the period of training are shown in Table 1. No sig-
nificant difference was observed in the pretraining values
between the groups. For the NR group only, body mass
FIGURE 1—Acute changes in blood lactate, growth hormone, andtestosterone concentrations after exercises with the NR and WR reg-
imens before the period of training. Values are means SE ( N 9).* Significant difference from preexercise value ( P< 0.05); # significantdifference between the regimens ( P < 0.05).
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Values are means SE. Pre and post indicate the values obtained before and after thetraining period, respectively. ** Significant difference from pretraining value (P 0.01);† significant difference from CON group (P 0.05); †† significant difference from CON
group (P 0.01).
FIGURE 2—Acute changes in epinephrine and norepinephrine con-centrations after exercises with the NR and WR regimens before theperiod of training. Values are means SE ( N 9). * Significant
difference from preexercise value ( P < 0.05); # significant differencebetween the regimens ( P < 0.05).
FIGURE 3—Percent changes in muscle cross-sectional area (CSA)after exercise training in the no-rest regimen (NR; N 9), regimen
with a rest period within a set (WR; N 9), and untrained (CON; N
8) groups. Values are means SE; ** significant difference betweenthe groups ( P < 0.01).
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The changes in force–velocity relationships after the
training period are shown in Figure 5. All values of isomet-
ric and isokinetic torques were normalized to the pretraining
values of isometric torque. The NR group showed signifi-
cant increases in isometric and isokinetic strengths at almost
all velocities examined, whereas no significant changes
were observed in the WR and CON groups. When comparedbetween groups, isometric strength showed a significantly
greater increase in the NR group (19.1 3.1%) than in the
WR (7.2 3.2%) and CON (1.5 1.0%) groups. The
maximal isometric strength per unit of CSA did not signif-
icantly change after the training period in both the NR (3.6
0.2 vs 3.8 0.2 Nmcm2, NS) and WR (3.6 0.2 vs
3.7 0.2 Nmcm2, NS) groups. In addition, no significant
difference was seen in the percent changes of maximal
isometric strength per unit of CSA between the groups,
suggesting that the strength gain in NR group was caused
primarily by muscular hypertrophy.
Changes in muscular endurance. Muscular endur-ance was evaluated as the exercise volume performed at
70% of 1RM for the upper- and lower-limb muscles (Table
3 and Fig. 6). In the upper-limb muscles, no significant
changes were seen in the NR and WR groups after the
training period. In the lower-limb muscles, muscular endur-
ance in the NR and CON groups significantly improved
after training period, whereas that in the WR group did not.
In addition, the percent change in exercise volume was
significantly greater in the NR group (41.8 10.2%) than
in the WR (7.8 8.0%) and CON (5.9 1.7%) groups,
indicating that only the NR regimen was substantially ef-
fective in improving muscular endurance.
DISCUSSION
This study showed that a NR regimen caused larger
elevations of blood LA, GH, and NE concentrations than a
WR regimen. In addition, training with NR regimen caused
FIGURE 4—Changes in one-repetition maximum (1RM) of shoulderpress and bilateral knee extension exercises during and after a 12-wk
training period. Absolute values (left) and percent changes ( right) areshown. Values are means SE; ** significant difference from pre-training value ( P < 0.01); # significant difference from CON group
( P < 0.05); ## significant difference from CON group ( P < 0.01);†† significant difference between the groups ( P < 0.01).
FIGURE 5—Changes in force–velocity relationships after the period of training. All values of knee extension strength were normalized to the
pretraining values of isometric strength (0°s1). Values are means SE; * significant difference from pretraining value ( P < 0.05); ** sig-
nificant difference from pretraining value ( P < 0.01).
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much larger increases in muscle CSA and strength than with
the WR regimen, although both regimens had the same
relative intensity and volume. As these regimens were de-
signed to induce different metabolic responses, the specific
adaptations in these regimens may be related to differences
in exercise-induced metabolic stress.
The effects of the NR regimen in inducing elevations of
GH, E, and NE concentrations are consistent with previous
studies (12,23). However, the secretions of GH and NE were
abolished when a short rest period (30 s) was inserted in the
middle of an exercise set (WR regimen). The attenuation of
hormone responses in the WR regimen may result from a
smaller amount of metabolite accumulation within the mus-
cles, because the blood lactate concentration after the WR
regimen was significantly lower than after the NR regimen
(Fig. 1). Several studies have shown that accumulation of
metabolic subproducts stimulates the secretions of GH and
catecholamine through afferent signals from intramuscular
metaboreceptors (6,25,28). This is consistent with the pre-
vious studies that have shown that alkalosis treatment at-
tenuates exercise-induced GH secretion (6), and that isch-emic exercise with increased metabolite accumulation
causes greater GH and NE responses (25,29). Therefore, it
appears that intraset rest in the WR regimen reduces acidity
via lactate production, causing smaller GH and NE re-
sponses. However, activation of motor centers may also
directly stimulate the hypothalamus–pituitary axis and sym-
pathoadrenal secretion (11). A more fatiguing NR regimen
might cause a stronger activation of the motor center and
thereby larger hormonal responses. Moreover, the tradi-
tional measurements of GH concentration have focused only
on the main 22 kDa isoform, whereas recent studies have
shown that other isoforms of GH have specific responses toacute exercise (19). Further studies are needed to examine
changes in various GH isoforms after resistance exercise.
We hypothesized that a NR regimen with greater meta-
bolic stress would produce larger hormonal responses than
a WR regimen. However, this hypothesis was not supported
for TES, because both regimens failed to evoke a significant
TES response, suggesting that TES responses are not greatly
affected by exercise-induced metabolic changes. This is
partially consistent with finding that muscle ischemia
caused by vascular occlusion did not enhance the TES
response to acute exercise (29). TES secretion is also sup-
pressed for several hours after a single bout of strenuous
resistance exercise (18). However, in the present study,
measurements after the period of training showed small but
significant elevations of postexercise TES concentration
(preexercise: 626.8 15.6 ngdL1 vs mean of postexer-
cise: 687.9 21.9 ngdL1
, P 0.01). These changes inacute TES responses might play a significant role in train-
ing-induced muscular adaptations (2).
The percent changes in 1RM and maximal isometric
strength were significantly greater in the NR group than in the
WR group (Figs. 4 and 5). In addition, maximal isokinetic
strength improved at almost all angular velocities in the NR
group, but not in the WR and CON groups (Fig. 5). Rooney et
al. (20) have shown a greater increase in dynamic strength in
a regimen with repeated six repetitions without rest compared
with a regimen with a 30-s rest period between each repetition.
Similarly, Schott et al. (21) have demonstrated that gains in
strength resulting from isometric training with long, fatiguing
FIGURE 6—Percent changes in work volume during shoulder press
and bilateral knee extension exercises at 70% of 1RM after the periodof training in the NR, WR, and CON groups. Values are means SE;* significant difference between the groups ( P < 0.05).
TABLE 3. Changes in exercise volume during shoulder press and knee extensionexercises at 70% of 1RM after the training period.
Values are means SE. Pre and post indicate the values obtained before and after thetraining period, respectively. Exercise volume was calculated as load number of
repetitions. * Significant difference from pretraining value (P 0.05); ** significantdifference from pretraining value (P 0.01); # significant difference from WR group (P
0.05); †† significant difference from CON group (P 0.01).
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contractions are considerably greater than with a training reg-
imen using shorter, intermittent contractions. The current and
previous results clearly indicate that continuous repetition
without pause is an important factor for strength gains follow-
ing resistance training.
The present NR regimen caused an increase of approxi-
mately 13% in muscle CSA, whereas the WR regimen had
no such effect (Fig. 3). Recent studies have suggested that
enhanced metabolic stress within the muscles may strongly
stimulate protein synthesis and concomitant muscle hyper-
trophy (21,26,27). For example, Schott et al. (21) have
shown that an isometric training regimen with a greater
decrease in intramuscular pH could induce a larger degree of
muscle hypertrophy than that with a smaller pH change.
Takarada et al. (26) have also shown that resistance exercise
with moderate vascular occlusion provokes a marked in-
crease in muscle CSA, and that this effect is related in part
to the increase in muscle fiber recruitment by acidic intra-
muscular environment. During exercise with marked meta-
bolic changes, additional motor unit recruitment would be
induced to keep a given level of force, as shown by the
elevated electrical activity of the muscles 17). In the present
study, although electrical activity was not measured, we
speculate that greater metabolic stress in the NR regimen
would have affected muscle fiber recruitment. This might be
responsible for the larger muscular hypertrophy in the NR
regimen.
As shown in Figure 1, significant elevations of postexer-
cise GH concentration were seen only in the NR regimen.
Although the actual roles of circulating anabolic hormones
in muscle growth are still unclear, combinations of GH and
mechanical loading would activate anabolic processes in
skeletal muscle (15). The acute elevation of GH has been
suggested to play a more significant role in increasinginsulin-like growth factor-1 (IGF-1) mRNA in the muscle
than do its chronic changes (9). In addition, lines of evi-
dence have indicated that GH and IGF-1 play crucial roles
in the growth, development, and maintenance of skeletal
muscle. In the present study, the magnitude of the acute GH
responses showed a positive correlation with relative in-
creases in muscle CSA (P 0.04–0.05), implying that GH
might contribute to exercise-induced muscular hypertrophy.
However, actions of GH for muscular hypertrophy are not
direct, and might be mediated by locally produced growth
factors (5). More research should be conducted to determine
whether GH plays a substantial role in resistance training–induced muscular hypertrophy.
Elevations of resting hormone concentrations may also be
related to muscular adaptations to resistance training. Pre-
vious studies have shown positive correlations between
changes in resting TES concentration and both muscular
strength development (2,10) and hypertrophy (8). However,
the present resting concentrations of GH, TES, IGF-1, and
cortisol did not change after the period of exercise training
in the NR group (data not shown).
Interestingly, a different adaptation in muscular endur-
ance was observed between the upper and lower limbs. In
the lower limbs, improvement in muscular endurance was
significantly greater in the NR group than in the WR and
CON groups, whereas that in the upper limb was not regi-
men-dependent (Fig. 6). The reason for this is unclear, but
previous studies have suggested that upper-limb muscles
have a greater trainability than lower-limb muscles that are
more involved in daily physical activities (1). Therefore, a
considerable improvement in muscular endurance of the
upper limb might take place even after the WR regimen with
intraset rest period. The interpretation of muscular endur-
ance data for knee extension needs precaution, because the
work volume in the CON group increased after the period of
training, possibly because of some familiarization with the
testing. Despite this fact, however, the improvement of work
volume during knee extension was much larger in the NR
group than in the WR and CON groups.
In conclusion, the NR regimen, consisting of moderate
intensity and short interset rest periods, evoked strong LA,
GH, E, and NE responses, and was also effective in increas-
ing muscular size and strength after a period of training. In
contrast, both acute and long-term effects were markedly
diminished when a brief rest period was inserted into each
set of exercise. These results suggested that resistance ex-
ercise-induced metabolic stress was associated with acuteGH, E, and NE responses and chronic muscular adaptations.
Moreover, these indicated that reducing rest periods to in-
crease metabolic stress was an effective strategy for gaining
substantial effects of resistance exercise. Development of
resistance exercise regimens designed to produce muscular
hypertrophy should take this phenomenon into account.
The authors are grateful to the subjects who participated in thisstudy. We are also grateful to Dr. Kaneko for assisting with the MRImeasurements, and Dr. Kraemer for his constructive comments.
The study was supported by grants from the Ministry of Educa-tion, Science, Sports and Culture of Japan, and from the ResearchFellowships of the Japan Society for the Promotion of Science forYoung Scientists.
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