Cadore et al. 2012 AGE

Full text

Neuromuscular adaptations to concurrent training
in the elderly: effects of intrasession exercise sequence
Eduardo Lusa Cadore &Mikel Izquierdo &
Stephanie Santana Pinto &Cristine Lima Alberton &
Ronei Silveira Pinto &Bruno Manfredini Baroni &
Marco Aurélio Vaz &Fábio Juner Lanferdini &Régis Radaelli &
Miriam González-Izal &Martim Bottaro &
Luiz Fernando Martins Kruel
Received: 21 December 2011 /Accepted: 16 March 2012
#American Aging Association 2012
Abstract The aim of this study was investigate the
effects of different intrasession exercise orders in the
neuromuscular adaptations induced by concurrent
training in elderly. Twenty-six healthy elderly men
(64.7±4.1 years), were placed into two concurrent
training groups: strength prior to (SE, n013) or after
(ES, n013) endurance training. Subjects trained
strength and endurance training during 12 weeks,
three times per week performing both exercise types
in the same training session. Upper and lower body
one maximum repetition test (1RM) and lower-body
isometric peak torque (PTiso) and rate of force devel-
opment were evaluated as strength parameters. Upper
and lower body muscle thickness (MT) was deter-
mined by ultrasonography. Lower-body maximal sur-
face electromyographic activity of vastus lateralis and
rectus femoris muscles (maximal electromyographic
(EMG) amplitude) and neuromuscular economy (nor-
malized EMG at 50 % of pretraining PTiso) were
determined. Both SE and ES groups increased the
upper- and lower-body 1RM, but the lower-body
1RM increases observed in the SE was higher than
ES (35.1± 12.8 vs. 21.9 ± 10.6 %, respectively; P<
0.01). Both SE and ES showed MT increases in all
muscles evaluated, with no differences between
groups. In addition, there were increases in the maxi-
mal EMG and neuromuscular economy of vastus lat-
eralis in both SE and ES, but the neuromuscular
economy of rectus femoris was improved only in SE
(P<0.001). Performing strength prior to endurance
exercise during concurrent training resulted in greater
lower-body strength gains as well as greater changes
in the neuromuscular economy (rectus femoris)in
elderly.
Keywords Combined training .Electromiography .
Muscle thickness .Aerobic exercise .Resistance
exercise
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DOI 10.1007/s11357-012-9405-y
E. L. Cadore :S. S. Pinto :C. L. Alberton :R. S. Pinto :
B. M. Baroni :M. A. Vaz :F. J. Lanferdini :R. Radaelli :
L. F. M. Kruel
Exercise Research Laboratory, Physical Education School,
Federal University of Rio Grande do Sul,
Porto Alegre, RS, Brazil
M. Izquierdo :M. González-Izal
Department of Health Sciences,
Public University of Navarre,
Navarre, Spain
M. Bottaro
College of Physical Education, University of Brasília,
Brasília, DF, Brazil
C. L. Alberton
Sogipa Physical Education and Sports College,
Porto Alegre, RS, Brazil
E. L. Cadore (*)
LAPEX, Escola de Educação Física, UFRGS,
Rua: Felizardo, 750, Bairro: Jardim Botânico,
90690-200 Porto Alegre, RS, Brazil
e-mail: edcadore@yahoo.com.br

Introduction
Biological aging is associated with declines in the
muscle mass, strength performance, and cardiorespi-
ratory fitness resulting in an impaired capacity of
elderly performing daily activities (Izquierdo et al.
2001,2003; Aagaard et al. 2010). To counteract this
effect, a combination of strength and endurance train-
ing in elderly populations is the most effective strategy
to improve both neuromuscular and cardiorespiratory
functions and consequently to maintain the functional
capacity during aging (Wood et al. 2001; Izquierdo et
al. 2004; Cadore et al. 2011b). However, strength and
endurance training have specific cardiovascular and
neuromuscular adaptations that are opposite in nature.
The primary adaptations to strength training include
enhanced strength performance (García-Pallarés and
Izquierdo 2011), muscle cell hypertrophy (Kraemer
et al. 1995), and neural adaptations such as the in-
crease in the maximal motor unit recruitment (Knight
and Kamen 2001), maximal motor unit firing rate
(Kamen and Knight 2004), as well as elevated spinal
motorneuronal excitability and increased efferent
motor drive (Aagaard et al. 2002a,b), with no changes
in VO
2max
. In contrast, endurance training induces
central and peripheral adaptations that enhance
VO
2max
and the ability of skeletal muscle to generate
energy via oxidative metabolism with no increase in
muscle strength or hypertrophy (Izquierdo et al. 2004).
Previous studies suggest that the simultaneous
performance of both types of training (i.e., concurrent
training) might reduce the strength development mag-
nitude when compared with that observed due to
strength training alone, and this phenomenon has been
called the “interference effect”(Sale et al. 1990;
Kraemer et al. 1995; Bell et al. 1997; Cadore et al.
2010; García-Pallarés and Izquierdo 2011).
A limited number of studies, however, have ex-
plored the neuromuscular adaptations related to con-
current strength and cardiovascular intervention in
elderly populations (Wood et al. 2001; Izquierdo et
al. 2004; Cadore et al. 2010;Holvialaetal.2010;
Karavirta et al. 2011). Wood et al. (2001)demonstrated
in elderly men that 12 weeks of concurrent training
resulted in similar strength gains to those observed
with strength training alone. However, the authors of
that study used 50 % lower volume of strength training
in the concurrent training group. Similarly, Izquierdo
et al. (2004) observed no differences in strength gain
between strength (twice weekly) and concurrent train-
ing (strength exercises on one day, cycle ergometer on
the other). Studies that have used similar volumes of
training between strength and concurrent groups in
elderly men have shown no interference effect after
21 week or concurrent training (Holviala et al. 2010;
Karavirta et al. 2009) whereas greater strength gains
were reported after strength training alone (67 %)
compared with the concurrent group (41 %) after 12-
week concurrent intervention (Cadore et al. 2010).
This controversial result may be related with the fact
of performing endurance exercises immediately prior
to strength exercises, which might have resulted in a
peripheral fatigue that consequently reduced perfor-
mance during strength training. In fact, it has been
shown that aerobic exercise might acutely reduce
strength performance (Lepers et al. 2001). If this were
the case, the interference effect could be avoided by
manipulating the intrasession exercise sequence.
Along with the scarce results regarding the influ-
ence of intrasession exercise sequence manipulation
on concurrent strength and endurance adaptations, to
the authors’best knowledge, there are no data regard-
ing the effect of exercise order manipulation during
concurrent training on the neural and muscle morphol-
ogy adaptations in elderly subjects. Such data would
give insight into possible mechanisms underlying the
chronic negative influence of endurance training in
strength training adaptation. Therefore, the purpose
of the present study was to investigate the effects of
different intrasession exercise orders during concur-
rent strength and endurance training on neuromuscular
adaptations in the elderly. Our hypothesis was that
performing strength exercise before endurance exer-
cise would result in greater strength increases than in
the opposite sequence (endurance strength).
Methods
Experimental design and approach to the problem
The physiological effects of different intrasession
exercise sequences during concurrent training in the
elderly were assessed with a strength and endurance
training protocol that, in previous studies by our
research group, have induced marked strength and
cardiovascular gains in this population (Cadore et
al. 2010,2011b). Because the performance of the
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concurrent training caused an interference effect on
strength adaptations, it was speculated that this effect
was a consequence of the fatigue resulting from en-
durance exercise, which was always performed imme-
diately before the strength exercise (Cadore et al.
2010). Thus, in the present study, we compared differ-
ent intrasession exercise sequences during concurrent
training in the same population (i.e., healthy elderly
subjects). The subjects were evaluated using variables
related to maximal strength, neuromuscular activity,
and muscle thickness. The concurrent training pro-
grams lasted 12 weeks. However, to test the stability
and reliability of the performance variables, some of
the subjects were evaluated twice before the start of
training (weeks −4 and 0), which served as a control
period. We have previously tested the stability and
reliability of these variables in elderly men using a
larger number of subjects during a control period
(Cadore et al. 2010,2011a,b). Each specific test at
pre- and post-intervention was overseen by the same
investigator, who was blinded to the training group of
the subjects, and was conducted on the same equip-
ment with identical subject/equipment positioning.
Each subject performed the tests at the same time of
day throughout the study, and different tests were
conducted on different days to avoid fatigue.
Subjects
Twenty-six healthy elderly men (mean±SD: 64.7±
4.1 years), who were not engaged in any regular and
systematic training program in the previous 12 months,
volunteered for the study after completing an ethical
consent form. Some of the participants had little previ-
ous experience with resistance or aerobic exercise. The
subjects volunteered for the present investigation fol-
lowing announcements in a widely read local newspa-
per. Subjects were carefully informed about the design
of the study with special information given regarding
the possible risks and discomfort related to the proce-
dures. Subsequently, subjects were randomly selected
and placed into two groups: strength training prior to
endurance training (SE, n013); and, endurance training
prior to strength training (ES, n013). Eight subjects
(66.0±2.7 years) were evaluated twice before the start
of training (weeks −4 and 0) and it served as control
period. The study was conducted according to Declara-
tion of Helsinki and was approved by Ethics Committee
of Federal University of Rio Grande do Sul, Brazil.
Exclusion criteria included any history of neuro-
muscular, metabolic, hormonal, and cardiovascular
diseases. Subjects were not taking any medication
with influence on hormonal and neuromuscular me-
tabolism and were advised to maintain their normal
dietary intake throughout the study. Medical evalua-
tions were performed using clinical anamnesis and
effort electrocardiograph test, to ensure subject suit-
ability for the testing procedure. The physical charac-
teristics of subjects are shown in Table 1. Body mass
and height were measured using an Asimed analog
scale (resolution of 0.1 kg) and an Asimed stadiometer
(resolution of 1 mm), respectively. Body composition
was assessed using the skinfold technique. A
seven-site skinfold equation was used to estimate
body density (Jackson and Pollock 1978)andbody
fat was subsequently calculated using the Siri
equation (Siri 1993).
Maximal dynamic strength
Maximal strength was assessed using the one-
repetition maximum test (1RM) on the bilateral elbow
flexion and bilateral knee extension. The bilateral
elbow flexion 1RM was performed with free weights
and using a bar and the bilateral knee extension in an
exercise machine (World-Esculptor, Porto Alegre,
Brazil). One week prior to the test day, subjects were
familiarized with all procedures in two sessions. On
the test day, the subjects warmed up for 5 min on a
cycle ergometer, stretched all major muscle groups,
and performed specific movements for the exercise
test. Each subject’s maximal load was determined with
no more than five attempts with a 4-min recovery
between attempts. Performance time for each contrac-
tion (concentric and eccentric) was 2 s, controlled by
an electronic metronome (Quartz, CA, USA). The
test–retest reliability coefficient (intraclass correlation
coefficient, ICC) was 0.99 for the knee extension and
0.95 for the elbow flexion.
Isometric peak torque and rate of force development
Maximal isometric peak torque was obtained using
and isokinetic dynamometer (Biodex, New York,
USA). Subjects were positioned seated with their hips
and thighs firmly strapped to the seat of the dynamom-
eter, with the hip angle at 85°. After that, subjects
warmed up for 10 knee extension/flexion repetitions
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at angular velocity of 90°s
−1
, performing a submaxi-
mal effort. The dynamometer was connected to an A/
D converter (Dataq Instruments Inc., Akron, OH,
USA), which made it possible to quantify the torque
exerted when each subject executed the knee exten-
sion at the determined angle. After having their right
leg positioned by the evaluators at an angle of 120° in
the knee extension (180° represented the full exten-
sion), the subjects were instructed to exert maximum
strength possible as fast as was possible when extend-
ing or flexing the right knee. The subjects had three
attempts at obtaining the maximum voluntary contrac-
tion (MVC) of the knee extensors and more three of
the knee flexors, each lasting 5 s. After the MVCs, in
order to evaluate the isometric neuromuscular econo-
my, subjects had three 5-s attempts to exert 50 % of
the pretraining isometric peak torque and maintain it
for, at least, 3 s receiving a visual feedback in the
computer that showed, in real-time, the force values.
If the subjects had success in the first trial, the last two
was not performed. The rest of the interval between
each attempt of the protocol was 2 min. During all the
maximum tests, the researchers provided verbal en-
couragement so that the subjects would feel motivated
to produce their maximum force. The force–time
curve was obtained using Biodex software with an
acquisition rate of 2,000 Hz. Signal processing includ-
ed filtering with a Butterworth low-pass filter of fourth
order at a cutoff frequency of nine Hertz. Maximal
peak torque was defined as the highest value of the
torque (Newton meter) recorded during the unilateral
knee extension and flexion. The isometric force–time
analysis on the absolute scale included the maximal
rate of force development (RFD; Newton per second),
defined as the greatest increase in the force; and, the
RFD at 100 ms, defined as the greatest increase in the
force in the first period of 100 ms. The RFD variables
were calculated from the force onset, which was con-
sidered the point that the force exceeded 2.5 times the
standard deviations of the mean of the force signal at
rest, and were determined using the MATLAB soft-
ware. The test–retest reliability coefficients (ICC)
were over 0.94 for all the variables in the isometric
protocol.
EMG measurements
During the isometric strength test, the maximal neuro-
muscular activity of agonist muscles was evaluated
using surface electromyography (RMS values) in the
vastus lateralis and rectus femoris, and the antagonist
co-activation in the biceps femoris long head. Electro-
des were positioned on the muscular belly in a bipolar
configuration (20 mm interelectrode distance) in par-
allel with the orientation of the muscle fibers, accord-
ing to Leis and Trapani (2000). Shaving and abrasion
with alcohol were carried out on the muscular belly, as
previously described by Häkkinen et al. (2003), in
order to maintain the interelectrodes resistance above
of 2,000 Ω. To ensure the same electrode position in
subsequent tests, the right thigh of each subject was
mapped for the position of the electrodes moles and
small angiomas by marking on transparent paper
(Narici et al. 1989). The ground electrode was fixed
on the anterior crest of the tibia. The raw EMG signal
was acquired simultaneously with the MVC using an
eight-channel electromyograph (AMT-8, Bortec Bio-
medical Ltd., Canadá). The raw EMG was converted
by an A/D converter DI-720 with 16-bits resolution
(Dataq Instruments Inc. Akron, OH, USA), with a
Table 1 Physical characteristics before and after training; mean±SD
Strength–endurance group SE, n013 Endurance–strength group ES, n013
Pre Post Pre Post
Age (years) 64.7± 3.7 64.9± 3.9 64.7± 4.8 64.8 ± 4.8
Body mass (kg) 79.7±10.5 79.5± 9.5 83.3± 13.4 82.6± 13.3
Height (cm) 170.0± 5.9 170.0 ±5.9 173.5± 5.1 173.5± 5.1
% Fat mass 27.3±3.7 25.6±3.3
a
28.1± 3.0 26.8 ± 3.4
a
VT
2
(ml kg min
−1
) 19.7± 3.9 20.5± 3.2 19.9± 4.9 20.0 ± 4.7
VO
2peak
(ml kg min
−1
) 27.4± 6.1 29.5± 6.6
a
26.6± 6.9 28.8 ± 6.5
a
a
Significant difference from pretraining values (P<0.001)
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sampling frequency of 2,000 Hz per channel, connected
to a PC. Following acquisition of the signal, the data
were exported to the SAD32 software, where they were
filtered using the Butterworth band-pass filter of fourth
order, with a cutoff frequency between 20 and 500 Hz.
After that, the EMG records were sliced exactly in 1 s
when maximal value of stable force (1 second) was
determined between the second and fourth second of
the force–time curve, and the RMS values were calcu-
lated. The RMS values of the antagonist biceps femoris
muscle were normalized by the maximum RMS values
of this muscle, obtained during the highest MVC of
isometric knee flexion at 100°.
After determination of maximal neuromuscular ac-
tivity, submaximal neuromuscular activity was evalu-
ated in order to determine the isometric neuromuscular
economy. Thus, subjects performed the force trials
corresponding to 50 % of pretraining MVC (described
above). The apparatus and the collection and analysis
procedures were the same used to determine the max-
imal EMG signal. After the training period, the sub-
maximal neuromuscular activity was determined for
the same absolute loads used in the pretraining evalu-
ation. The submaximal RMS values were normalized
using the maximum RMS values obtained during the
MVC in each muscle. The test–retest reliability coef-
ficient (ICC values) of the EMG measurements was
over 0.85.
Muscle thickness
The muscle thickness (MT) was measured using B-
mode ultrasound (Philips, VMI, MG, Brazil). A 7.5-
MHz scanning head was placed on the skin perpen-
dicular to the tissue interface, the scanning head was
coated with a water-soluble transmission gel to pro-
vide acoustic contact without depressing the dermal
surface. The images were digitalized and after ana-
lyzed in software Image-J (National Institutes of
Health, USA, version 1.37). The subcutaneous adi-
pose tissue–muscle interface and the muscle–bone
interface were identified, and the distance from the
adipose tissue–muscle interface was defined as MT.
The MT images were determined in the lower body
muscles vastus lateralis (VL), vastus medialis (VM),
vastus intermedius (VI), and rectus femoris (RF). The
measurement for the VL was taken at midway be-
tween the lateral condyle of the femur and greater
trochanter (Kumagai et al. 2000; Miyatani et al.
2002), whereas the measurement VM was taken at
30 % of the distance between the lateral condyle of
the femur and the greater trochanter (Korhonen et al.
2009), yet the measurement for the VI and RF were
measured as 60 % the distance from the greater tro-
chanter to the lateral epicondyle and 3 cm lateral to the
midline of the anterior thigh (Chilibeck et al. 2004).
The sum of the four lower body muscles MT was
considered as representative of quadríceps femoris
(QF) muscle mass. In the upper body limbs, MT were
obtained in the bíceps brachii (BB) and brachialis
(BR) and the sum of the MT of these muscles was
considered as representative of elbow flexors (EF)
muscle mass. The site to EF measurement was at
40 % of the distance from the lateral epicondyle to
the acromion process of the scapula, starting at the
lateral epicondyle (Miyatani et al. 2002; Fukunaga et
al. 2001). To ensure the same electrode position in
subsequent tests, the right thigh of each subject was
mapped for the position of the electrodes moles and
small angiomas by marking on transparent paper
(Narici et al. 1989). Subjects were evaluated in supine
position, after 15-min resting and after 72 h without
any vigorous physical activity. The MT test–retest
reliability coefficients (ICC) were 0.92 for BB, 0.93
for BR, 0.94 for VL, 0.91 for VM, 0.92 for VI, and
0.95 for RF.
Peak oxygen consumption and ventilatory threshold
Subjects performed an incremental test on a cycle
ergometer (Cybex, USA) in order to determine the
peak oxygen consumption (VO
2peak
) heart rate (HR
VT
)
at ventilatory threshold (VT
2
). They initially cycled
with a 25 W load, which was progressively increased
by 25 W every 2 min, while maintaining a cadence of
70–75 rpm, until exhaustion (Izquierdo et al. 2004).
The test was halted when subjects were no longer able
to maintain a cadence of over 70 rpm. All the incre-
mental tests were conducted in the presence of a
physician. The expired gas was analyzed using a met-
abolic cart (CPX/D, Medical Graphics Corporation,
St. Paul, MN, USA) breath by breath. The VT
2
was
determined using the ventilation curve corresponding
to the point of exponential increase in the ventilation
in relation to the load. In addition, to confirm the data,
VT
2
was determined using the CO
2
ventilatory equiv-
alent (Wasserman 1986). The maximum VO
2
value
(milligram per kilogram per minute) obtained close
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to exhaustion was considered the VO
2peak
. The maxi-
mum test was considered valid if at least two of the
three listed criteria were met: (1) the maximum heart
rate predicted by age was reached (220, age); (2) the
impossibility of continuing to pedal at a minimum
velocity of 70 rpm; and (3) an RER greater than 1.1
was obtained (Bell et al. 1997,2000). Three experi-
enced, independent physiologists determined the
corresponding points. For the data analysis, the curves
of the exhaled and inhaled gases were smoothed by
visual analysis using the software Cardiorespiratory
Diagnostic Software Breeze Ex version 3.06. The
heart rate (HR) was measured using a Polar monitor
(model FS1, Shangai, China). The test–retest reliabil-
ity coefficients (ICC) were 0.88 for VO
2peak
and 0.85
for VT
2
.
Concurrent training programs
Participants of the study trained both strength and
endurance training in the same session, three times a
week, on nonconsecutive days. Training groups were
differentiated by their intrasession concurrent strength
and endurance training sequence. One group trained
the strength training prior to SE, and another trained
endurance prior to ES. Strength training was designed
to improve muscular endurance in the first 4 weeks
and subsequently to stimulate muscular hypertrophy
and maximal strength gains. Before the start of the
strength training, subjects completed two familiariza-
tion sessions to practice the exercises they would
further perform during the training period. The
strength and endurance training programs have been
previously described (Cadore et al. 2010,2011a). The
individuals performed nine exercises (bench press,
inclined leg-press, seated row, knee extension, inverse
fly, leg curl, triceps curl, biceps curl, and abdominal
exercises). In each session, subjects performed specif-
ic muscle stretching and a specific warm up, with one
set of 25 repetitions with very light loads for the upper
and lower body. During weeks 1 and 2, subjects per-
formed two sets of 18–20 repetitions maximum (RM)
in week 1 (i.e., the heaviest possible weight was used
for the designated number of repetitions; mean±DP of
relative load, 39.8±7.4 % of pretraining 1RM), pro-
gressing to 15–17 RM (week 3; 48.3±5.7 % of pre-
training 1RM). In weeks 5–7, subjects performed two
sets of 12–14 RM (64.1±8.7 % of pretraining 1RM),
progressing to three sets of 8–10 RM (weeks 8–10)
(81.3±12.3 % of pretraining 1RM), advancing to 6–
8 RM (weeks 11–12; 93.1± 14 % of pretraining 1RM).
During the training program, the maximal training
load of the knee extensors exercises in each mesocycle
(i.e., 18–20, 15–17, 12–14, 8–10, and 6–8 RM) was
recorded to allow future comparisons between groups.
However, relative to 1RM loads were not controlled
during the training program. In each set, the workload
was adjusted when the repetitions performed were
either above or below the repetitions established. All
the sets were performed until failure. The recovery
time between sets was 90–120 s. The strength training
sessions lasted approximately 40 min.
The endurance training program was performed,
using a cycle ergometer, at the intensity relative to
the HR
VT
corresponding to the second VT
2
. During
the first 2 weeks, subjects cycled for 20 min at 80 % of
HR
VT
, progressing to 25 min at 85–90 % of HR
VT
in
weeks 5–6. In the weeks 7–10, subjects cycled for
30 min at 95 % of HR
VT
and in the last 2 weeks of
training, subjects performed six 4-min bouts at 100 %
of HR
VT
(weeks 11–12), with 1 min of active recovery
between bouts. The VT
2
, used as a parameter to pre-
scribe the intensity of endurance training, corre-
sponded to 73.8± 4.9 % of the VO
2peak
. All the
training sessions were carefully supervised by at least
three experienced personal trainers.
Statistical analysis
The SPSS statistical software package was used to
analyze all data. Normal distribution and homogeneity
parameters were checked with Shapiro–Wilk and
Levene tests, respectively. Results are reported as
mean±SD. Statistical comparisons in the control
period (from weeks −4 to 0) were performed by using
Student’spairedttests. The training-related effects
were assessed using a two-way analysis of variance
(ANOVA) with repeated measures (group ×time). To
verify changes in the training load peak, Bonferroni
post hoc test was used after two-way ANOVA. Selected
relative changes between groups were compared via
one-way ANOVA. The sample size was calculated
using the G POWER software (version 3.0.1) that
determined that a sample of n013 subjects, would
provided a statistical power of over 0.85 in all varia-
bles. The retrospective statistical power provided by
SPSS after analysis was 1.00 in all strength perfor-
mance variables which a significant time–effect was
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observed and 0.8 for the significant time vs. group
interaction results. Exceptions were observed in the
RFD at 100 ms and maximal RFD, which the retro-
spective statistical power was 0.71 and 0.78, respec-
tively. Furthermore, the retrospective statistical power
in the EMG variables were 0.8 and 0.92 for the
maximal EMG amplitude of VL and RF, respectively;
and 1.0 and 0.85 for VL and and RF neuromuscular
economy, respectively. Significance was accepted
when p<0.05.
Results
During the period control (i.e., between weeks −4 and
0), no changes were observed in the lower-body 1RM
(63.9±10.3 vs. 64.1±10.2 kg), maximal neuromuscu-
lar activity of VL (0.180±0.075 vs. 0.197±0.094 V)
and RF (0.121±0.081 vs. 0.161±0.010 V), as well as
in the VO
2peak
(28.7±3.8 vs. 27.6±3.6 ml kg min
−1
).
There were no differences between groups before
training in the body mass (kilogram), height (centime-
ter), age (years), and percent fat (percentage). After
training, there was a significant decrease in the percent
of body fat in both SE and ES (27.3± 3.7 vs. 24.8± 4.3 %
and 28.1±2.9 vs. 26.8±3.4 %, respectively, P<0.001)
with no differences between groups (Table 1). No
changes were observed in the body mass after training.
Training compliance and maximal training load
of a specific training period (mesocycle)
There was no difference in the training compliance
between SE and ES (94.8±4.3 vs. 97.2±2.9 %). Dur-
ing the different mesocycles, there was strong trend
toward time vs. group interaction in the maximal
training load relative to pretraining 1RM values in
the knee extension exercise (P00.056; Fig. 1) with
the SE showing higher relative increases in this vari-
able than ES during the strength training periodization
[149.1±37.7 % (from 38.7±5 to 95±10 % of pretrain-
ing 1RM) vs. 132.9±32.2 % (from 36.2±10 to 82.9±
8 % of pretraining 1RM), respectively].
Dynamic strength
At baseline, there were no differences between groups
in the lower- and upper-body 1RM. After training,
there was significant time vs. group interaction (P<
0.02) in the lower-body 1RM. Both SE and ES in-
creased the knee extensors 1RM values, but the in-
crease observed in the SE was significantly higher
than ES (35.1±12.8 vs. 21.9±10.6 %, respectively,
P<0.01). In the upper-body 1RM, there were sig-
nificant increases in both SE and ES (15.0± 9.0 vs.
11.5± 7.3 %, respectively, P<0.001), with no differ-
ence between groups (Fig. 2).
Isometric peak torque and rate of force development
At baseline, there were no differences between groups
in the isometric peak torque of knee extensors and
flexors, knee extensors maximal RFD, or RFD at
100 ms. After training, there were increases in the
knee extensors isometric peak torque in both SE and
Fig. 1 Mean± SD of maximal training load (percentage) rela-
tive to pretraining one maximum repetition maximum (1RM)
values during different mesocycles. Tendency toward significant
time vs. group interaction (P00.056)
Fig. 2 Mean± SD of lower-body one maximum repetition
(1RM) values (kilogram), pre- and post-12 weeks of concurrent
training. SE strength prior to endurance training, ES endurance
prior to strength training. *P<0.001, significant difference from
pretraining values. †P<0.001, significant time vs. group
interaction
AGE

ES (8.0±7.1 vs. 5.7±9.6 %, respectively, P<0.001),
with no difference between groups. In addition, knee
flexors isometric peak torque increased in both SE and
ES (7.8±8.7 vs. 7.9±7.7 %, respectively, P<0.001),
with no difference between groups. There were
increases in the knee extensors RFD at 100 ms in both
SE and ES (P<0.05), as well as in the knee extensors
maximal RFD in SE and ES groups (P<0.001), with
no differences between groups (Table 2).
Muscle thickness
At baseline, there were no differences between groups
in the lower- (VL, RF, VM, VI, and QF sum) and
upper-body muscle thickness (BB, BR, and EF sum;
Table 3). After training, there was increases in the VL
(SE, 7.3±4.6 %; ES, 7.5±5.3 %; P<0.001), VM (SE,
16.7±14.2 %; ES, 9.7±8.3 %; P<0.001), VI (SE, 9.4±
8.7 %; ES, 12.1±9.3 %; P<0.001), and RF muscle
thickness (SE, 3.5±3.2 %; ES, 6.4± 3.8 %; P<0.001),
with no differences between groups. In addition, there
was increases in the QF sum (SE, 9.3±6.2 %; ES, 9.0±
5.0 %; P<0.001), with no differences between groups
(Fig. 3). In the upper-body muscle thickness, there was
increases inthe BB (SE, 4.6±3.7 %; ES, 3.3±1.9 %; P<
0.001), BR (SE, 13.5±7.5 %; ES, 9.1±10.8 %; P<
0.001), and EF sum (SE, 7.0±2.8 %; ES, 5.0±3.5 %;
P<0.001). No differences between groups were ob-
served in the upper-body muscle thickness variables.
EMG measurements
At baseline, there were no differences between groups
in the maximal neuromuscular activity (maximal
EMG amplitude) of VL, RF, maximal coactivation of
BF, as well neuromuscular economy of VL and RF.
After training, there were significant increases in the
maximal neuromuscular activity of VL (SE, 16.7±
40.5 %; ES, 18.3±21.2 %; P<0.05; Fig. 4), as well
as RF (SE, 22.5±23.6 %; ES, 14.1±26.2 %, P<0.01;
Fig. 5), with no differences between groups. There
were no changes in the coactivation of BF during the
knee extensors MVC after training in any group
(Table 3). After training, there was significant time
vs. group interaction (P<0.01) in the RF neuromuscu-
lar economy. Changes were observed only in SE
(−22.6±30.0 %, P<0.01), and this change was greater
(P<0.01) than the observed in ES (1.5±24.0 %, P0
0.86; Fig. 6). There were changes in the VL neuromus-
cular economy (SE, −16.9±12.7 %; ES, −12.5±15.4 %;
P<0.001), with no differences between groups.
Discussion
The primary finding of the present study was the
greater lower-body strength gains observed when
strength training was performed prior to endurance
training (i.e., SE) compared with those observed when
the endurance training was performed prior to strength
training. Secondly, the greater strength gains in the SE
sequence may be related with neural adaptations be-
cause only SE improved the rectus femoris neuromus-
cular economy. Furthermore, no differences were
observed in the morphological adaptations between
groups, which suggested that the intrasession exercise
sequence influenced strength performance but not the
magnitude of hypertrophy. These results suggest that
Table 2 Strength performance before and after training: strength–endurance (SE) and endurance–strength (ES); mean±SD
Strength–endurance (SE, n013) Endurance–strength (ES, n013)
Pre-training Post-training Pre-training Post-training
Upper-body 1RM (kg) 27.0±2.2 31.3± 3.7
***
26.2± 4.2 29.1 ± 4.4
***
Lower-body 1RM (kg) 68.1± 9.8 91.5 ±12.7
***, ****
72.7± 11.8 88.3±14.9
***
KE isometric PT (Nm) 229.8± 27.8 247.3±26.9
***
238.6± 38.6 250.2 ± 34.3
***
KF isometric PT (Nm) 116.6±15.0 125.0± 15.6
***
115.1±25.7 131.9±40.0
***
KE RFD at 100 ms (Nm s
−1
) 490.6± 354.0 620.0 ± 366.8
*
428.7± 320.0 652.5 ± 459.5
*
KE maximal RFD (Nm s
−1
) 773.7± 354.4 879.7 ± 434.9
**
757.7± 324.5 1,007.2 ± 515.9
**
1RM one maximum repetition, KE knee extensors, KF knee flexors, PT peak torque, RFD rate of force development
*P<0.05, **P< 0.01, ***P< 0.001, significant difference from pretraining values; ****P< 0.05, significant time vs. group interaction
AGE

performing strength training prior to endurance train-
ing optimizes strength gains in the elderly.
In the present study, both the ES and SE interven-
tiongroupsshowedstrengthgains(22and35%,
respectively) at a similar or greater magnitude com-
pared with those observed in other studies that have
investigated strength versus concurrent training adap-
tations in the elderly (20–41 %) (Wood et al. 2001;
Izquierdo et al. 2004; Holviala et al. 2010,2011;
Karavirta et al. 2009,2011). In Holviala et al.
(2010), 21 weeks of strength or concurrent training
resulted in similar strength gains in elderly men (20
Table 3 Muscle thickness, maximal neuromuscular activity and neuromuscular economy before and after training: strength–endurance
(SE) and endurance–strength (ES); mean±SD
Strength–endurance (SE, n013) Endurance–strength (ES, n013)
Pretraining Post-training Pretraining Post-training
VL muscle thickness (mm) 19.8 ±2.7 21.3± 3.2
***
21.6± 2.3 23.2 ± 2.3
***
VM muscle thickness (mm) 19.3± 2.9 22.5±3.9
***
19.4± 4.7 21.2 ± 5.1
***
VI muscle thickness (mm) 14.3±3.4 15.6± 3.5
***
14.8± 4.1 16.4 ± 3.9
***
RF muscle thickness (mm) 18.6±3.8 19.1±3.8
***
17.6± 3.6 19.0 ± 3.4
***
QF muscle thickness (mm) 72.0±8.6 78.5± 8.7
***
73.4± 10.5 79.8 ± 10.8
***
BB muscle thickness (mm) 25.5±3.8 26.7± 4.2
***
25.9± 4.2 26.7 ± 4.0
***
BR muscle thickness (mm) 9.4± 1.9 10.7±2.2
***
10.4± 2.6 11.3±3.0
***
EF muscle thickness (mm) 34.9 ± 2.8 37.4±3.0
***
36.3± 4.6 38.1 ± 4.4
***
Maximal NA VL (V) 0.189± 0.093 0.204± 0.087
*
0.143± 0.065 0.168 ± 0.077
*
Maximal NA RF (V) 0.120± 0.038 0.143 ±0.043
**
0.096± 0.040 0.109 ± 0.050
**
Antagonist coactivation BF (%) 21.4± 11.4 19.8± 10.1 24.2± 10.7 27.3±18.3
Neuromuscular economy VL (%) 42.3± 8.0 34.9±7.6
***
44.2± 8.9 38.4 ± 9.3
***
Neuromuscular economy RF (%) 41.9± 11.9 31.1± 11.8
**, ****
38.3± 12.3 37.8 ± 11.8
Maximal neuromuscular activity (NA) determined by maximal electromiographic signal amplitude
VL vastus lateralis, VM vastus medialis, VI vastus intermedius, RF rectus femoris, BF bíceps femoris
*P<0.05, **P< 0.01, and ***P<0.001, significant difference from pretraining values; ****P<0.05, significant time vs. group
interaction
Fig. 3 Mean ± SD of the quadriceps femoris muscle thickness
(millimeter) pre- and post-12 weeks of concurrent training. SE
strength prior to endurance training, ES endurance prior to
strength training. *P< 0.001, significant difference from pre-
training values
Fig. 4 Mean± SD of maximal neuromuscular activity (maximal
electromiographic amplitude) of vastus lateralis (RMS values)
pre- and post-12 weeks of concurrent training. SE strength prior
to endurance training, ES endurance prior to strength training.
*P<0.05, significant difference from pretraining values
AGE

and 21 %). In another study, Karavirta et al. (2011),
using a similar strength training regime, demonstrated
strength enhancements of similar magnitudes after
21 weeks of strength training alone or concurrent
training (21–22 %). It is interesting to note that the
same strength adaptations observed in the present
study occurred in a shorter period of time than in the
abovementioned studies (12 vs. 21 weeks; Holviala et
al. 2010,2011; Karavirta et al. 2009,2011). These
different time courses in strength development could
be explained by the different weekly frequency of
training performed. The subjects of the present study
performed three training sessions per week, which is
in contrast with the previous studies, which utilized
two training sessions per week (Holviala et al. 2010,
2011; Karavirta et al. 2011). The increased number of
training sessions in our study represents a 50 % higher
volume of training. Thus, it is possible that the higher
weekly volume performed in the present study might
explain such neuromuscular adaptations as were
observed here after only 12 weeks, even when
performing endurance training immediately prior to
strength training.
A unique finding was that greater strength increases
were observed in the group that performed strength
training prior to endurance training. Few studies have
investigated the effects of intrasession exercise se-
quence on the neuromuscular adaptations to concur-
rent training. In the study of Gravelle and Blessing
(2000), which investigated young women, no signifi-
cant differences were observed in the strength adapta-
tions between groups that performed different exercise
sequences. In another study, Chtara et al. (2008) ob-
served an interference effect on the strength gains in
young men after 12 weeks of concurrent training but
no effect of different intrasession sequences (i.e.,
strength–endurance vs. endurance–strength). Using a
concurrent training regime identical to the present
study, Cadore et al. (2010) found that strength training
alone resulted in a 50 % greater increase in knee
extensor strength than concurrent training in a similar
population (i.e., healthy untrained elderly people). In
that study, because the endurance training was always
performed immediately before strength training, it was
hypothesized that the fatigue resulting from endurance
exercise may have negatively affected the training-
induced muscle strength gains. Therefore, the extent
to which different intrasession exercise sequences
(i.e., strength–endurance or endurance–strength)
would result in different neuromuscular adaptations
in the elderly was hypothesized. The results of the
present study are in line with the results of Cadore et
al. (2010) because in the present study, SE increased
the maximal dynamic strength 50 % more than that
observed after an ES order. A plausible explanation
was that performing endurance training immediately
prior to strength training might negatively influence
the subsequent strength training performance. In this
context, one may also suggest that the lower strength
gains obtained after the ES training approach could be
related in part to the fact that the ES group also
achieved lower workloads in the training periodization
(Fig. 1). It should also be noted that differences in the
Fig. 5 Mean± SD of maximal neuromuscular activity (maximal
EMG amplitude) of rectus femoris (RMS values) pre- and post-
12 weeks of concurrent training. SE strength prior to endurance
training, ES endurance prior to strength training. *P<0.05,
significant difference from pretraining values
Fig. 6 Mean ± SD of neuromuscular economy (normalized
EMG at 50 % of pretraining MVC) of rectus femoris before
and after training in strength group (SG). *P<0.01, significant
difference from pretraining values; †P<0.01, significant time
vs. group interaction
AGE

relative intensity of workloads between groups were
more evident in the last two training cycles, when the
volume per exercise during the strength training was
between 10 and 6 RM, and the endurance intensity
was close to VT
2
.
In the present study, both groups increased the muscle
thicknessof the elbow flexor and knee extensor muscles.
Some studies have shown that a high volume of concur-
rent training might impair the hypertrophy of type I
fibers (Kraemer et al. 1995; Bell et al. 1997,2000;
Putman et al. 2004). Nevertheless, studies using imaging
techniques to evaluate muscle hypertrophy have shown
no differences in the magnitude of increase in muscle
size between strength and concurrent groups in young
(McCarthy et al. 2002; Häkkinen et al. 2003; Izquierdo
et al. 2005), as well in elderly untrained subjects
(Izquierdo et al. 2004; Sillampää et al. 2008;Karavirta
et al. 2011). The present results are in agreement with
those from previous studies that have found increases in
the muscle thickness induced by strength training or
concurrent training (Sillampää et al. 2008; Nogueira et
al. 2009; Ahtiainen et al. 2010). Furthermore, it seems
that performing endurance training before or after
strength training in the same concurrent training session
has no influence on the magnitude of the muscle hyper-
trophy induced by strength training. One might specu-
late that even performing strength training with a lower
relative loading intensity (percent of 1RM), the use of
maximal effort per set allows the ES group to stimulate
its optimal contractile protein synthesis, which results in
the same level of morphological adaptation. Indeed, it
has been extensively shown in the literature that the
optimal strength development stimulus is not necessarily
the same as the optimal muscle hypertrophy stimulus
(Schoenfeld 2010). It should be stated that potential
differences in overall muscle size between ES and SE
could be detected using imaging techniques with better
spatial resolution (i.e., magnetic ressonance image and
computadorized tomography).
Increases in the maximal EMG amplitude of the VL
and RF muscles were observed in SE and ES, suggesting
that both groups may be an optimal stimulus to enhance
the neuromuscular activity (Häkkinen et al. 2003;
Brentano et al. 2008). In contrast, performing strength
training prior to endurance training resulted in a greater
magnitude of neuromuscular economy (i.e., a reduction
in the normalized EMG signal at the same absolute load)
of the rectus femoris muscle in the SE group, whereas
both groups improved the neuromuscular economy of
vastus lateralis muscle. It could be speculated that the
greater improvements in the neuromuscular economy in
SE, together with the absence of differences in the
morphological adaptations (i.e., muscle thickness) be-
tween groups, suggest that neural factors may help ex-
plain the different magnitude of strength gains, with the
endurance training session performed immediately be-
fore strength exercises negatively influencing such adap-
tations. Impairments in the neural adaptations induced
by concurrent training have been demonstrated by
Häkkinen et al. (2003) and Cadore et al. (2010), who
show that only strength training alone results in
increases in rapid neural activation (Häkkinen et al.
2003) and maximal neuromuscular activity (Cadore et
al. 2010) when compared with concurrent training. In
addition, Cadore et al. (2010) have shown improve-
ments in neuromuscular economy only in the elderly
that performed strength training alone. However, caution
is necessary in the interpretation of the present results
because neuromuscular activity was evaluated isometri-
cally and the different magnitude of strength gains was
detected in a dynamic strength test (i.e., 1RM). More-
over, only one EMG parameter was more improved in
SE than ES group. Thus, the interference of the intra-
session exercise order in the neural adaptations as a
mechanism to explain the different strength gains in
the present study needs be further investigated. Further-
more, it is also possible that the greater magnitude of the
neuromuscular economy enhancements observed in SE
could be a consequence of the greater strength gains
rather than a cause of those gains. An improved neuro-
muscular economy suggests that for the same pretrain-
ing load, subjects needed fewer motor units after
training, being more economical at the neuromuscular
level (Cadore et al. 2010,2011a,b). Despite differences
between groups, both SE and ES have improved the
neuromuscular economy to some extent.
To conclude, the present data expand the knowledge
of previous findings related to the interference effect
observed during concurrent training in an elderly popu-
lation. The intrasession exercise sequence had an influ-
ence on strength adaptations as observed in the greater
strength increases when strength training was performed
prior to endurance training (35 vs. 22 %). These differ-
ences might be related to the different training load peak
achieved between groups, especially during the later
phase of training, which the endurance training was
performed close to the anaerobic ventilatory threshold.
Furthermore, a different magnitude of neural adjustment
AGE

might be suggested as a possible physiological explana-
tion for these different strength adaptations because the
neuromuscular economy was improved to a greater
extent in the group that performed strength training
prior to endurance training, whereas no differences
between groups were observed in the maximal neuro-
muscular activity gains. Nevertheless, in the elderly, it
is important to point out that the intrasession concur-
rent exercise sequence had no influence on muscle
thickness gains. From a practical point of view, to
optimize the strength gains in the elderly, the concur-
rent training prescription should include an intrases-
sion exercise order of strength training prior to
endurance training.
Acknowledgments The authors specially thank FAPERGS,
CAPES, CNPq, and FINEP Brazilian Government Associations
for support to this project. The authors are also indebted to the
Spanish Ministry of Health, Institute Carlos III, Department of
Health of the Government of Navarra and the Government of
Spain, and the Spanish Ministry of Science and Innovation for
financing this research with grants RD06/013/1003 and 87/2010
and DEP2011-24105, respectively. We also acknowledge Mr.
Matheus Conceição, Dr. Giovani Cunha, and Prof. Guilherme
Trindade for their help in data collection and analysis. Furthermore,
we also gratefully acknowledge all subjects who participated in this
research and made this project possible.
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