InclinacaodobanconosupinoalteraaativacaoEMG

Prévia do material em texto

Journal of Electromyography and Kinesiology 67 (2022) 102722
Available online 25 October 2022
1050-6411/© 2022 Elsevier Ltd. All rights reserved.
Non-uniform excitation of pectoralis major induced by changes in bench 
press inclination leads to uneven variations in the cross-sectional area 
measured by panoramic ultrasonography 
José Carlos dos Santos Albarello a, Hélio V. Cabral b,*, Bruno Felipe Mendonça Leitão a, 
Gustavo Henrique Halmenschlager a, Tea Lulic-Kuryllo b, Thiago Torres da Matta a 
a Laboratório de Biomecânica Muscular, Escola de Educação Física e Desportos, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil 
b Department of Clinical and Experimental Sciences, Università degli Studi di Brescia, Brescia, Italy 
A R T I C L E I N F O 
Keywords: 
Chest press variations 
Muscle architecture 
Resistance training 
Surface electromyography 
A B S T R A C T 
This study combined surface electromyography with panoramic ultrasound imaging to investigate whether non- 
uniform excitation could lead to acute localized variations in cross-sectional area and muscle thickness of the 
clavicular and sternocostal heads of pectoralis major (PM). Bipolar surface electromyograms (EMGs) were ac-
quired from both PM heads, while 13 men performed four sets of the flat and 45◦ inclined bench press exercises. 
Before and immediately after exercise, panoramic ultrasound images were collected transversely to the fibers. 
Normalized root mean square (RMS) amplitude and variations in the cross-sectional area and muscle thickness 
were calculated separately for each PM head. For all sets of the inclined bench press, the normalized RMS 
amplitude was greater for the clavicular head than the sternocostal head (Parchitecture after 
the training session. If there is an association between regional excita-
tion and inhomogeneous muscle adaptation, as previously suggested via 
magnetic resonance images (Wakahara et al., 2012; Wakahara et al., 
2013), we would expect that the pectoralis major head with the greatest 
sEMG amplitude during exercise will be the one with the greatest acute 
variations in muscle architecture. 
2. Material and Methods 
2.1. Participants 
Thirteen male, resistance-trained participants (mean ± standard 
deviation: age 28.79 ± 4.46 years; height 174.64 ± 5.60 cm; body mass 
79.43 ± 8.99 kg) were recruited to participate in the study. Participants 
were recruited from the staff and student population at the Federal 
University of Rio de Janeiro. Female participants were not included due 
to breast tissue overlying the sternocostal head, hampering the acqui-
sition of panoramic ultrasound images. All participants were free from 
upper limb and trunk musculoskeletal injuries in the last 12 months. 
Participants were classified as resistance-trained based on two inclusion 
criteria: (i) to have resistance training experience greater than or equal 
to 12 months and (ii) to be able to perform one repetition maximum 
(1RM) of the flat bench press exercise with a load of at least 100 % of 
their body mass (Lauver et al., 2016). In addition, all participants per-
formed only resistance training as physical activity. After being 
informed about the experimental procedures, all subjects provided 
written informed consent. This study was conducted in accordance with 
the latest version of the Declaration of Helsinki and approved by the 
ethics committee of the Hospital Universitário Clementino Fraga Filho 
(HUCFF/UFRJ; CAAE number: 29820120.9.0000.5257). 
2.2. Experimental protocol 
The study consisted of four experimental sessions. The first three 
were separated by at least 72 h and the third and fourth by at least 96 h. 
The interval of 96 h was adopted between sessions three and four to 
minimize any possible effects of exercise-induced muscle damage 
(Meneghel et al., 2014). On the first visit, participants were familiarized 
with the experimental procedures and performed a 1RM test for two 
bench press exercise inclinations, flat and inclined (45◦). On the second 
visit, the 1RM test was reassessed to obtain the reliability measurements. 
In the last two visits, the participants performed four sets of the flat and 
inclined bench press, one exercise each day. The exercise order was 
randomized, and a rest period of at least 3 min was provided between 
the sets. During the experimental period, participants abstained from 
any strenuous activity involving the upper or lower limbs (Trebs et al., 
2010). 
2.3. Measures 
2.3.1. 1RM and exercise protocol 
The 1RM test was applied to determine the load used in the flat and 
inclined bench press exercises. During the test, the bar (10 kg) center 
was maintained over the middle of sternum length for the flat bench 
press and just above the nipple line for the inclined bench press. The 
handgrip width adopted was 150 % of biacromial distance (Lauver et al., 
2016). A 30-min rest interval was provided between flat and inclined 
bench press 1RM tests. Participants warmed up by performing four sets 
of 20, 12, 6, and 1 repetition with a load intensity, respectively, of 30 %, 
50 %, 70 %, and 85 % of their estimated 1RM (Coratella et al., 2020), 
with 1 min rest in-between (Muyor et al., 2019). Three minutes 
following the warm-up, they performed the first attempt of 1RM test. 
The maximum load was defined when the participant was able to 
perform one valid repetition but failed to achieve the second. The 
movement was considered valid when the participant touched the bar 
against their chest and, subsequently, moved the bar until reaching the 
full elbow extension, completing a full range of motion (Lauver et al., 
2016). If the participant successfully completed the second repetition, 
the load was increased from 4 to 10 kg for the next attempt. For each 
condition (flat and 45◦ inclined), a maximum of five attempts were 
performed with a 5-minute rest interval in between (adapted from (Il 
et al., 2012)). For the exercise protocol, participants warmed up by 
performing one set of 10 repetitions with a load of 50 %-1RM. After two 
minutes of rest, they were instructed to perform four sets of the flat or 
45◦ inclined bench press exercises using a load corresponding to 60 
%-1RM. Participants performed each set until the exercise failure, 
defined as the time point when they could no longer keep the movement 
cadence. The number of repetitions in each exercise set was stored for 
further analysis. A metronome was used to control the exercise cadence 
with 2 s for each concentric and eccentric phase (Coratella et al., 2020). 
2.3.2. Electrodes positioning and surface EMG recordings 
Two pairs of adhesive electrodes (30 mm interelectrode distance, 
Spesmedica, Genoa, Italy) were positioned on the clavicular and ster-
nocostal heads of the pectoralis major muscle to sample the sEMG during 
the flat and inclined bench press exercises. First, the length of the ster-
num was defined as the distance between the manubrium (0 %) and the 
xiphoid process (100 %), both identified by palpation. Moreover, the 
insertion of the pectoralis major into the intertubercular sulcus of the 
humerus was identified and marked on the skin with the aid of a B-mode 
ultrasound (Linear transducer of 40 mm; 12 MHz; gain 60 dB; deep 4 cm; 
Logic, Healthcare, USA). A reference line to guide the electrode place-
ment on the sternocostal head was then traced (Fig. 1A), connecting the 
point at 50 % of the sternum length to the insertion of the pectoralis 
major (Mancebo et al., 2019). For the clavicular head, the ultrasound 
transducer was positioned transversely to the pectoralis major fibers at 
50 % of the clavicle length and the aponeurosis separating the two 
J.C.S. Albarello et al. 
Conteúdo licenciado para Ivna -
Journal of Electromyography and Kinesiology 67 (2022) 102722
3
pectoralis major heads was located and marked on the skin (Fig. 1B). A 
reference line to guide the electrode location on the clavicular head was 
drawn in parallel to the clavicle and in the region between the identified 
aponeurosis and the clavicle (Fig. 1A). The ultrasound transducer was 
further used to check whether the reference lines were parallel to the 
orientation of the clavicular and sternocostal pectoralis major fascicles. 
The electrode pairs were positioned over the clavicular and sterno-
costal reference lines (Fig. 1A) in the region between the sternum and 
the pectoralis major innervation zone. For the innervation zone identi-
fication, a dry array of sixteen silver-bar electrodes (10 mm inter- 
electrode distance; LISiN-Politecnico di Torino, Turin, Italy) aligned 
parallel to the reference lines was used in a procedure previously 
detailed by Mancebo and colleagues (Mancebo et al., 2019). Briefly, the 
single-differential sEMG were visually inspected while the participants 
were asked to hold the bar in the initial position of the bench press 
exercise. When necessary, the dry array orientation was slightly modi-
fied until the propagation of action potentials could be clearly observed 
across the electrodes (Fig. 1C). The innervation zones were then visually 
identified as the channel (pair of electrodes) with small EMG amplitude 
and located between two channels providing action potentials with 
phase opposition (Mancebo et al., 2019; Fig. 1C). Before positioning the 
bipolar electrodes, the skin of the participants was shaved, lightly 
abraded, and cleaned with alcohol. In order to reposition the electrodes 
in the same location across different days,a transparent paper map was 
used to mark the reference lines and anatomical landmarks (i.e., ma-
nubrium and xiphoid process) for each participant. Bipolar sEMG were 
digitized at a sampling frequency of 2048 Hz using a 16-bit A/D con-
verter (gain 200; common-mode rejection ratio > 100 dB; DuePro EMG; 
LISiN and OTBioelettronica, Turin, Italy) and transmitted via wireless 
(Bluetooth) to a portable computer. The vertical acceleration of the 
barbell was acquired using a triaxial accelerometer (acceleration range 
of ± 8 g; sampling frequency of 100 Hz; 16-bit resolution; DueBio EMG, 
LISiN and OTBioelettronica, Turin, Italy). 
2.3.3. Ultrasound imaging 
Ultrasound B-mode panoramic images were acquired by the same 
experienced examiner. Two images were acquired before and two after 
the bench press exercises. First, participants were instructed to lie in a 
supine position on a padded bed with their shoulders abducted at 90◦
and externally rotated for better visualization of the pectoralis major 
lateral tendon on the ultrasound images. Panoramic images were then 
collected transversely to the pectoralis major fibers (Fig. 2A). Specif-
ically, the midpoint of the clavicle was identified and marked on the skin 
(Kikuchi & Nakazato, 2017; Yasuda et al., 2010,) and the panoramic 
images were acquired from this point to the lower edge of the pectoralis 
major. Therefore, the ultrasound images encompassing the clavicular 
and sternocostal heads were obtained, as illustrated in Fig. 2B. The 
transducer path was guided by custom-made support to minimize po-
tential oscillations (Fig. 2A). Moreover, the same transparent paper map 
used for electrode re-positioning was used to guide the anatomical 
landmark identification on different days. A water-based gel was used 
for acoustic coupling, and the ultrasound acquisition configuration (60 
dB gain and 10 MHz operating frequency) was kept the same during all 
sessions and for all participants. Conversely, the depth and focus settings 
were adjusted for each participant to ensure the complete visualization 
of the pectoralis major deep aponeurosis. 
2.4. Ultrasound image and EMG processing 
For each pectoralis major head, the degree of muscle activity during 
Fig. 1. Electrodes’ placement. A, shows the reference lines used to position the electrodes pair in the pectoralis major clavicular (upper) and sternocostal heads 
(bottom). B, shows the ultrasound image acquire from pectoralis major muscle to identify the aponeurosis dividing the clavicular and sternocostal heads. C, shows the 
EMGs acquired using an array of 16 electrodes to identify the innervation zone (gray rectangle) of the pectoralis major muscle. The electrodes were then positioned 
far from the innervation zone. 
J.C.S. Albarello et al. 
Conteúdo licenciado para Ivna -
Journal of Electromyography and Kinesiology 67 (2022) 102722
4
the flat and 45◦ inclined bench press exercises was estimated from the 
root mean square (RMS) amplitude of surface sEMG. First, the bipolar 
sEMG were bandpass filtered with a fourth-order Butterworth filter 
(15–350 Hz cut-off frequencies). After that, the concentric and eccentric 
phases across bench press cycles were identified from the barbell 
vertical acceleration using a custom-written Matlab script (The Math-
Works Inc., Natick, Massachusetts, USA). Specifically, concentric and 
eccentric phases were identified, respectively, from local maxima to 
local minima and vice versa (Fig. 3A). The RMS amplitude of the 
clavicular and sternocostal heads was then computed over 90 % of the 
Fig. 2. Ultrasound image acquisition. A, shows 
de midclavicular reference line from where the 
panoramic transversal images were collected 
with the aid of a custom-made support. B, shows 
a panoramic ultrasound image encompassing 
both the clavicular and sternocostal heads. Both 
the cross-sectional area (dotted lines) and muscle 
thickness (left–right arrows) of the clavicular 
(blue) and sternocostal (yellow) regions were 
measured from this image. (For interpretation of 
the references to colour in this figure legend, the 
reader is referred to the web version of this 
article.) 
Fig. 3. A, shows the acceleration data from the barbell used to segment the concentric and eccentric phases. B, shows raw EMGs acquired from clavicular and 
sternocostal heads segmented by each phase. To eliminate the effects of myoelectric manifestation of fatigue as a confounder, only the EMGs acquired from 
concentric phases in which the phase duration was consistent with the average duration of the first two concentric phases of the set were considered. C, shows the 
interval considered to compute the root mean square (RMS) amplitude, which was 90% of the duration of the concentric phase. 
J.C.S. Albarello et al. 
Conteúdo licenciado para Ivna -
Journal of Electromyography and Kinesiology 67 (2022) 102722
5
duration of each concentric phase, such that the periods, including the 
transition between phases, were discarded (Cabral et al., 2022; Fig. 3C). 
Only RMS values of concentric phases in which the phase duration was 
consistent with the average duration of the first two concentric phases of 
the set were retained for further analysis. This was performed to elimi-
nate the effects of myoelectric manifestation of fatigue as a confounder 
(Merletti, Knaflitz & De Luca, 1990). Specifically, when two consecutive 
concentric phases had a duration higher or lower than 10 % of the 
average duration of the first two concentric phases of the set, they and 
the subsequent phases were excluded from the analysis (Fig. 3B). The 
RMS values of the considered concentric phases were then normalized 
by the highest RMS amplitude identified for the clavicular and sterno-
costal heads during the set. Thus, the normalization procedure was 
performed separately for each set (i.e., in each set we adopted a new 
RMS amplitude as reference), and the same reference value of the set 
was used for the clavicular and sternocostal regions. This procedure was 
performed separately for each bench press variation. The normalized 
RMS values were averaged across cycles. 
The public domain software ImageJ (National Institutes of Health, 
USA, v.1.43) was used to measure the ultrasound variables. The cross- 
sectional area and muscle thickness were used to assess the volume 
changes in the clavicular and sternocostal heads after the bench press 
exercises. The same evaluator analysed all ultrasound images. After 
changing the brightness and contrast of each ultrasound image to 
facilitate the visualization of anatomical structures, the aponeurosis 
separating the two pectoralis major heads was identified and marked in 
the image. The cross-sectional areas of clavicular and sternocostal heads 
were then traced and measured without including any other tissues 
(Fig. 2B). Additionally, muscle thickness of the sternocostal head was 
calculated as the perpendicular distance from the interface between 
muscle and adipose tissue to the interface between muscle and the third 
rib (yellow double arrow in Fig. 2B). The third rib was chosen because it 
was the approximate location of bipolar EMG electrodes overlaying the 
sternocostal head. For the clavicular head, the muscle thickness was 
quantified at the thickest part of the clavicular head for each image (blue 
double arrow in Fig. 2B). The average of muscle thickness and cross- 
sectional area between the two panoramic images acquired was 
considered for further analysis. For both the cross-sectional area and the 
muscle thickness,the percent variance was calculated as the difference 
between the value after and the value before the exercise normalized by 
the value before the exercise, and these values were used for the sta-
tistical analysis. 
2.5. Statistical analysis 
The intraclass correlation coefficient (ICC) and the coefficient of 
variation (CV) were used to assess the inter-day reliability of the 1RM 
load and the ultrasound measurements (muscle thickness and cross- 
sectional area). The ICC values were calculated using the two-way 
mixed-effects model and absolute agreement definition (Koo & Li, 
2016) and interpreted by thresholds (poor: 0.00–0.39; fair: 0.40–0.59; 
good: 0.60–0.74; excellent: 0.75–1.00) (Cicchetti & Sparrow, 1981). The 
averaged CV across participants was calculated for each variable and 
interpreted as good if CV 10 % (Jennings et al., 2010). 
Parametric analysis was considered for inferential statistics after 
ensuring the data normality (Shapiro-Wilk test; P > 0.05 for all cases) for 
all parameters. Three-way repeated-measures ANOVA was applied to 
compare the main and interaction effect of the set (1 to 4), the two bench 
press inclinations (flat and 45◦ inclined) and the two regions (clavicular 
and sternocostal) on the normalized RMS. Two-way repeated-measures 
ANOVA was applied to compare the main and interaction effect of the 
two bench press inclinations and the two regions on the muscle thick-
ness variation and cross-sectional area variation. To compare the num-
ber of repetitions across the sets and between bench press inclinations, a 
two-way repeated-measures ANOVA was applied. Tukey’s post-hoc test 
was used for paired comparisons whenever the main effects were veri-
fied. All analyses were carried out with GraphPad Prism (Version 6) and 
IBM SPSS Statistics (Version 21), and the significance level was set at 5 
%. 
3. Results 
3.1. Reliability results and bench press exercise performance 
As reported in Table 1, all variables used to examine the inter-day 
reliability had an average ICC higher than 0.939, indicating excellent 
reliability. In addition, the CV values were lower than 5 % for all pa-
rameters (Table 1), indicating good values. 
The mean ± standard deviation number of repetitions in sets 1, 2, 3, 
and 4, was respectively 11.79 ± 1.93, 9.43 ± 1.28, 8.79 ± 1.37, and 
7.79 ± 1.78 for the flat bench press, and 11.57 ± 1.34, 9.43 ± 1.22, 7.93 
± 0.83, and 7.50 ± 0.85 for the inclined bench press. For both the flat 
and inclined bench press exercises, a significant decrease in the number 
of repetitions was observed in sets 2, 3 and 4 compared with set 1 
(Tukey’s post-hoc test; P7
quantified in the sternocostal head than in the clavicular head after the 
flat bench press exercise (difference of 11.06 % for muscle thickness; 
difference of 5.42 % for cross-sectional area; Tukey’s post-hoc test; Pmethodologically relevant for future studies using 
this technique. 
4.2. Is there an association between the regional activation in pectoralis 
major during bench press exercises and the acute variations in muscle 
architecture after exercises? 
Although several studies, particularly in sports and exercise sciences, 
presume a direct association between the magnitude of muscle excita-
tion, as inferred from surface EMG, and muscle structural adaptation, 
there is limited indirect evidence corroborating this association (for 
details, see Vigotsky et al. 2022). In the current study, we examined 
whether the pectoralis major region with the greatest sEMG amplitude 
during variants of bench press exercise would be the one with the 
highest acute variations in muscle architecture. Interestingly, as shown 
in Fig. 6B, our key results support our initial hypothesis that, at least 
acutely, there is an association between the localized excitation of the 
pectoralis major during the bench press exercises and the uneven cross- 
sectional area increases after exercises. This association between muscle 
activation during exercise and cross-sectional area increases after the 
exercise, both assessed using magnetic resonance imaging, was already 
observed in the leg muscles during the squat exercise (Ploutz-Snyder, 
Convertino & Dudley, 1995), as well as in the triceps brachii muscle 
during the lying triceps extension exercise (Wakahara et al., 2012). Of 
methodological relevance, we demonstrated that surface electromyog-
raphy combined with panoramic ultrasound imaging may be a useful 
and straightforward approach to investigate neuromuscular and struc-
tural adaptations to resistance exercises, at least when comparing 
different regions of the same muscle. Uneven variations in muscle ar-
chitecture observed in this study may be affected by the total volume 
performed in each bench press exercise. Indeed, as previously reported 
(Jenkins et al., 2015), increases in muscle cross-sectional area are 
greater when the number of repetitions performed is higher. In the 
current study, we controlled the resistance training experience of par-
ticipants, adopted a relative exercise intensity (% of repetition 
maximum), and controlled the cadence of movement to deal with this 
possible confounding factor. As demonstrated in our results, a similar 
number of repetitions was performed between the two bench press in-
clinations and, thus, our findings were not affected by the differences in 
exercise volume. 
Acute changes in muscle architecture after resistance exercises were 
used to draw inferences about the physiological active hyperemia 
induced by exercise, which is defined by the redirection of blood flow to 
the target muscle (Jenkins et al., 2015; Vieira et al., 2018; Csapo, Alegre 
& Baron, 2011). Although the present study did not measure the phys-
iological active hyperemia, the muscle thickness and cross-sectional 
area increases provide information about this phenomenon, as in-
creases in muscle volume are a result of greater blood flow to the 
exercised muscle, due to the higher demands for oxygen and nutrients as 
well as for metabolite removal (Joyner & Casey, 2015). Indeed, a sig-
nificant correlation between the absolute changes in plasma volume and 
the cross-sectional area were observed for different leg muscles after the 
squat exercise (Ploutz-Snyder, Convertino & Dudley, 1995). Hence, 
uneven increases in the cross-sectional area according to the bench 
inclination may be explained by the redirection of blood flow to the 
pectoralis major region with greater involvement during each exercise. 
Interestingly, when the same pectoralis major head was compared 
between the two exercises, no differences in the cross-sectional area 
increases were observed for the clavicular head. Thus, despite the higher 
muscle activity of the clavicular head in the inclined bench press 
compared with the flat bench press (Fig. 5), the acute structural adap-
tation was the same for both exercise variants (increases of ~ 23 % in 
cross-sectional area; Fig. 6B). Contrarily, greater increases in the cross- 
sectional area were observed for the sternocostal head during the flat 
compared with the inclined bench press exercise, which is consistent 
with the muscle activation results of this head. Although speculative, a 
potential explanation for these findings is that the activation of the 
clavicular head demanded during the flat bench press may be already 
sufficient to elicit the maximal increase in cross-sectional area, mainly 
considering that it is a narrow region of the pectoralis major. 
A final consideration on the local changes in the pectoralis major 
muscle architecture concerns the muscle thickness results. In contrast to 
the cross-sectional area, during the inclined bench press, there were no 
differences in muscle thickness increases between the clavicular and 
sternocostal heads. This divergence may be potentially explained by the 
representativeness of each measurement. While the cross-sectional area 
is a two-dimensional measurement encompassing a wide muscle region, 
the muscle thickness is a one-dimensional measurement at a single point 
in the muscle. Considering the possibility of regional structural varia-
tions following resistance training (Zabaleta-Korta, Fernández-Penã, 
Santos-Concejero, 2020), the changes in muscle thickness may not be 
representative of the changes occurring in the muscle (Franchi et al., 
2018). Therefore, we suggest using the cross-sectional area rather than 
muscle thickness to detect non-uniform changes within the muscle 
following resistance training exercises. 
Limitations. 
This study had several limitations. First, there is evidence suggesting 
the lower sternocostal region, which we did not examine, may play an 
important role in specific movements of the glenohumeral joint (Lulic- 
Kuryllo et al., 2021). However, the flat and inclined bench press exer-
cises primarily involve horizontal flexion and/or forward flexion, which 
typically activate the clavicular region and the central bundles of ster-
nocostal region (Cabral et al., 2022), and, therefore, we decided to focus 
on those regions. Second, heterogeneous variations in the muscle 
thickness of medio-lateral regions of pectoralis major were previously 
reported after the flat bench press exercise (Leitão et al., 2020). How-
ever, we decided to acquire the panoramic ultrasound images at 50 % of 
the clavicle length only, as pilot data showed that this location was the 
best one to identify the aponeurosis separating the clavicular and ster-
nocostal heads. 
5. Conclusion 
From a practical perspective, our results suggest that changes in 
bench press inclination induce a differential excitation of distinct pec-
toralis major regions. Furthermore, when comparing different heads of 
the pectoralis major for the same exercise variant, this preferential 
excitation is associated with uneven responses of cross-sectional area 
following the exercise. Thus, the manipulation of bench press inclination 
may be a useful strategy for coaches and practitioners to selectively 
stimulate the sternocostal and clavicular heads. Our findings also 
demonstrated that when controlling for spurious factors affecting the 
acquisition and interpretation of sEMG amplitudes, the conventional 
bipolar sEMG technique can provide reliable information of non- 
uniform regional muscle activation. However, our results allow us to 
make solely acute inferences. Future longitudinal studies are required to 
investigate whether the acute association between regional excitation 
and localized structural adaptations observed here may be transferred to 
J.C.S. Albarello et al. 
Conteúdo licenciado para Ivna -
Journalof Electromyography and Kinesiology 67 (2022) 102722
9
chronic adaptations (e.g., hypertrophy). 
Declaration of Competing Interest 
The authors declare that they have no known competing financial 
interests or personal relationships that could have appeared to influence 
the work reported in this paper. 
Acknowledgment 
This work was financially supported by the “Coordenação de Aper-
feiçoamento de Pessoal de Nível Superior (CAPES)”, the “Conselho 
Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”, the 
“Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio 
de Janeiro (FAPERJ)”, and the “Financiadora de Estudos e Projetos 
(FINEP).” 
References 
Ackland, D.C., Pak, P., Richardson, M., Pandy, M.G., 2008. Moment arms of the muscles 
crossing the anatomical shoulder. J Anat. 213, 383–390. https://doi.org/10.1111/ 
j.1469-7580.2008.00965.x. 
Ackland, D.C., Pandy, M.G., 2011. Moment arms of the shoulder muscles during axial 
rotation. J Orthop Res. 29 (5), 658–667. https://doi.org/10.1002/jor.21269. 
Barnett, C., Kippers, V., Turner, P., 1995. Effects of variations of the bench press exercise 
on the EMG activity of five shoulder muscles. J Strength Cond Res. 9, 222–227. 
https://doi.org/10.1519/00124278-199511000-00003. 
Cabral, H.V., de Souza, L.M.L., de Oliveira, L.F., Vieira, T.M., 2022. Non-uniform 
excitation of the pectoralis major muscle during flat and inclined bench press 
exercises. Scand J Med Sci Sport. 32, 381–390. https://doi.org/10.1111/sms.14082. 
Cicchetti, D.V., Sparrow, S.A., 1981. Developing criteria for establishing interrater 
reliability of specific items: applications to assessment of adaptive behavior. Am J 
Ment Defic. 86, 127–137. 
Coratella, G., Tornatore, G., Longo, S., Esposito, F., Cè, E., 2020. Specific prime movers’ 
excitation during free-weight bench press variations and chest press machine in 
competitive bodybuilders. Eur J Sport Sci. 20, 571–579. https://doi.org/10.1080/ 
17461391.2019.1655101. 
Csapo, R., Alegre, L.M., Baron, R., 2011. Time kinetics of acute changes in muscle 
architecture in response to resistance exercise. J Sci Med Sport. 14, 270–274. 
https://doi.org/10.1016/j.jsams.2011.02.003. 
De Luca, C.J., 1997. The use of surface electromyography in biomechanics. J Appl 
Biomech. 13, 135–163. 
De Luca, C.J., Merletti, R., 1988. Surface myoelectric signal cross-talk among muscles of 
the leg. Electroencephalogr Clin Neurophysiol. 69, 568–575. https://doi.org/ 
10.1016/0013-4694(88)90169-1. 
ElMaraghy, A.W., Devereaux, M.W., 2012. A systematic review and comprehensive 
classification of pectoralis major tears. J Shoulder Elb Surg. 21, 412–422. https:// 
doi.org/10.1016/J.JSE.2011.04.035. 
Franchi, M.V., Longo, S., Mallinson, J., Quinlan, J.I., Taylor, T., Greenhaff, P.L., 
Narici, M.V., 2018. Muscle thickness correlates to muscle cross-sectional area in the 
assessment of strength training-induced hypertrophy. Scand J Med Sci Sport. 28 (3), 
846–853. 
Fung, L., Wong, B., Ravichandiran, K., Agur, A., Rindlisbacher, T., Elmaraghy, A., 2009. 
Three-dimensional study of pectoralis major muscle and tendon architecture. Clin 
Anat. 22, 500–508. https://doi.org/10.1002/ca.20784. 
Gallina, A., Merletti, R., Gazzoni, M., 2013. Uneven spatial distribution of surface EMG: 
What does it mean? Eur J Appl Physiol. 113 (4), 887–894. https://doi.org/10.1007/ 
s00421-012-2498-2. 
Glass, S.C., Armstrong, T., 1997. Electromyographical Activity of the Pectoralis Muscle 
During Incline and Decline Bench Presses. J Strength Cond Res. 11, 163–167. 
Haładaj, R., Wysiadecki, G., Clarke, E., Polguj, M., Topol, M., 2019. Anatomical 
Variations of the Pectoralis Major Muscle: Notes on Their Impact on Pectoral Nerve 
Innervation Patterns and Discussion on Their Clinical Relevance. Biomed Res Int. 
2019, 13–15. https://doi.org/10.1155/2019/6212039. 
Hernández-Belmonte, A., Martínez-Cava, A., Pallarés, J.G., 2022. Pectoralis Cross- 
Sectional Area can be Accurately Measured using Panoramic Ultrasound: A Validity 
and Repeatability Study. Ultrasound Med Biol. 48, 460–468. https://doi.org/ 
10.1016/J.ULTRASMEDBIO.2021.10.017. 
Il, S.D., Kim, E., Fahs, C.A., et al., 2012. Reliability of the One-Repetition Maximum Test 
Based on Muscle Group and Gender. J Sports Sci Med. 11, 221. 
Inman, V.T., Saunders, J.B., Abbott, L.C., 1996. Observations of the function of the 
shoulder joint. 1944. Clin Orthop Relat Res. 330, 3–12. https://doi.org/10.1097/ 
00003086-199609000-00002. 
Jenkins, N.D.M., Housh, T.J., Bergstrom, H.C., et al., 2015. Muscle activation during 
three sets to failure at 80 vs. 30 % 1RM resistance exercise. Eur J Appl Physiol 115, 
2335–2347. https://doi.org/10.1007/S00421-015-3214-9. 
Jennings, D., Cormack, S., Coutts, A.J., Boyd, L., Aughey, R.J., 2010 Sep. The validity 
and reliability of GPS units for measuring distance in team sport specific running 
patterns. Int J Sports Physiol Perform. 5 (3), 328–341. https://doi.org/10.1123/ 
ijspp.5.3.328. 
Joyner, M.J., Casey, D.P., 2015. Regulation of increased blood flow (Hyperemia) to 
muscles during exercise: A hierarchy of competing physiological needs. Physiol Rev. 
95, 549–601. https://doi.org/10.1152/physrev.00035.2013. 
Kikuchi, N., Nakazato, K., 2017. Low-load bench press and push-up induce similar 
muscle hypertrophy and strength gain. J Exerc Sci Fit. 15, 37–42. https://doi.org/ 
10.1016/j.jesf.2017.06.003. 
Koo, T.K., Li, M.Y., 2016. A Guideline of Selecting and Reporting Intraclass Correlation 
Coefficients for Reliability Research. J Chiropr Med. 15, 155–163. https://doi.org/ 
10.1016/j.jcm.2016.02.012. 
Lauver, J.D., Cayot, T.E., Scheuermann, B.W., 2016. Influence of bench angle on upper 
extremity muscular activation during bench press exercise. Eur J Sport Sci. 16, 
309–316. https://doi.org/10.1080/17461391.2015.1022605. 
Leitão, B.F.M., de Oliveira, L.F., da Matta, T.T., 2020. Non-uniform acute variation 
among pectoralis major’s muscle thickness after bench press in trained men. Pensar a 
Prática. 23. https://doi.org/10.5216/rpp.v23.54690. 
Lulic-Kuryllo, T., Negro, F., Jiang, N., Dickerson, C.R., 2021. Standard bipolar surface 
EMG estimations mischaracterize pectoralis major activity in commonly performed 
tasks. J Electromyogr Kinesiol. 56, 102509 https://doi.org/10.1016/J. 
JELEKIN.2020.102509. 
Mancebo, F.D., Cabral, H.V., de Souza, L.M.L., de Oliveira, L.F., Vieira, T.M., 2019. 
Innervation zone locations distribute medially within the pectoralis major muscle 
during bench press exercise. J Electromyogr Kinesiol. 46, 8–13. https://doi.org/ 
10.1016/J.JELEKIN.2019.03.002. 
Meneghel, A.J., Verlengia, R., Crisp, A.H., Aoki, M.S., Nosaka, K., da Mota, G.R., 
Lopes, C.R., 2014. Muscle damage of resistance-trained men after two bouts of 
eccentric bench press exercise. J Strength Cond Res. 28 (10), 2961–2966. 
Merletti, R., Knaflitz, M., De Luca, C.J., 1990. Myoelectric manifestations of fatigue in 
voluntary and electrically elicited contractions. Myoelectric manifestations of 
fatigue in voluntary and electrically elicited contractions. 69 (5), 1810–1820. 
Muddle, T.W.D., Magrini, M.A., Colquhoun, R.J., Luera, M.J., Tomko, P.M., Jenkins, N.D. 
M., 2019. Impact of Fatiguing, Submaximal High- vs. Low-Torque Isometric Exercise 
on Acute Muscle Swelling, and Echo Intensity in Resistance-Trained Men. J Strength 
Cond Res. 33, 1007–1019. https://doi.org/10.1519/JSC.0000000000003033. 
Muyor, J.M., Rodríguez-Ridao, D., Martín-Fuentes, I., Antequera-Vique, J.A., Pessôa 
Filho, D.M., 2019. Evaluation and comparison of electromyographic activity in 
bench press with feet on the ground and active hip flexion. PLoS One. 14 (6), 
e0218209. https://doi.org/10.1371/JOURNAL.PONE.0218209. 
Paton, M.E., Brown, J.M.M., 1994. An electromyographic analysis of functional 
differentiation in human pectoralis major muscle. J Electromyogr Kinesiol. 4, 
161–169. https://doi.org/10.1016/1050-6411(94)90017-5. 
Ploutz-Snyder, L.L., Convertino, V.A., Dudley, G.A., 1995.Resistance exercise-induced 
fluid shifts: change in active muscle size and plasma volume. Am J Physiol. 269 (3 Pt 
2), R536–R543. https://doi.org/10.1152/AJPREGU.1995.269.3.R536. 
Rodríguez-Ridao, D., Antequera-Vique, J.A., Martín-Fuentes, I., Muyor, J.M., 2020. 
Effect of Five Bench Inclinations on the Electromyographic Activity of the Pectoralis 
Major, Anterior Deltoid, and Triceps Brachii during the Bench Press Exercise. Int J 
Environ Res Public Heal. 17, 7339. https://doi.org/10.3390/IJERPH17197339. 
Saeterbakken, A.H., Mo, D.A., Scott, S., Andersen, V., 2017. The Effects of Bench Press 
Variations in Competitive Athletes on Muscle Activity and Performance. J Hum 
Kinet. 57, 61–71. https://doi.org/10.1515/hukin-2017-0047. 
Smith, C.M., Housh, T.J., Herda, T.J., Zuniga, J.M., Ryan, E.D., Camic, C.L., 
Bergstrom, H.C., Smith, D.B., Weir, J.P., Cramer, J.T., Hill, E.C., Cochrane, K.C., 
Jenkins, N.D.M., Schmidt, R.J., Johnson, G.O., 2015. Effects of the innervation zone 
on the time and frequency domain parameters of the surface electromyographic 
signal. J Electromyogr Kinesiol. 25 (4), 565–570. 
Staudenmann, D., Kingma, I., Daffertshofer, A., Stegeman, D.F., van Dieën, J.H., 2009. 
Heterogeneity of muscle activation in relation to force direction: A multi-channel 
surface electromyography study on the triceps surae muscle. J Electromyogr 
Kinesiol. 19, 882–895. https://doi.org/10.1016/J.JELEKIN.2008.04.013. 
Terry, G.C., Chopp, T.M., 2000. Functional anatomy of the shoulder. J Athl Train. 35 (3), 
248–255. https://doi.org/10.1093/ptj/46.10.1043. 
Trebs, A.A., Brandenburg, J.P., Pitney, W.A., 2010. An electromyography analysis of 3 
muscles surrounding the shoulder joint during the performance of a chest press 
exercise at several angles. J Strength Cond Res. 24, 1925–1930. https://doi.org/ 
10.1519/JSC.0B013E3181DDFAE7. 
Vieira, A., Blazevich, A., Souza, N., Celes, R., Alex, S., Tufano, J.J., Bottaro, M., 2018. 
Acute changes in muscle thickness and pennation angle in response to work-matched 
concentric and eccentric isokinetic exercise. Appl Physiol Nutr Metab. 43 (10), 
1069–1074. 
Vigotsky, A.D., Halperin, I., Lehman, G.J., Trajano, G.S., Vieira, T.M., 2018. Interpreting 
signal amplitudes in surface electromyography studies in sport and rehabilitation 
sciences. Front Physiol. 8985 https://doi.org/10.3389/fphys.2017.00985. 
Vigotsky, A.D., Halperin, I., Trajano, G.S., Vieira, T.M., 2022. Vieira TM (2022) Longing 
for a Longitudinal Proxy: Acutely Measured Surface EMG Amplitude is not a 
Validated Predictor of Muscle Hypertrophy. Sport Med 52 (2), 193–199. 
Wakahara, T., Miyamoto, N., Sugisaki, N., Murata, K., Kanehisa, H., Kawakami, Y., 
Fukunaga, T., Yanai, T., 2012. Association between regional differences in muscle 
activation in one session of resistance exercise and in muscle hypertrophy after 
resistance training. Eur J Appl Physiol. 112 (4), 1569–1576. 
Wakahara, T., Fukutani, A., Kawakami, Y., Yanai, T., 2013. Nonuniform muscle 
hypertrophy: Its relation to muscle activation in training session. Med Sci Sports 
Exerc. 45, 2158–2165. https://doi.org/10.1249/MSS.0B013E3182995349. 
Watanabe, K., Kouzaki, M., Moritani, T., 2012. Task-dependent spatial distribution of 
neural activation pattern in human rectus femoris muscle. J Electromyogr Kinesiol. 
22, 251–258. https://doi.org/10.1016/J.JELEKIN.2011.11.004. 
J.C.S. Albarello et al. 
Conteúdo licenciado para Ivna -
https://doi.org/10.1111/j.1469-7580.2008.00965.x
https://doi.org/10.1111/j.1469-7580.2008.00965.x
https://doi.org/10.1002/jor.21269
https://doi.org/10.1519/00124278-199511000-00003
https://doi.org/10.1111/sms.14082
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0025
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0025
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0025
https://doi.org/10.1080/17461391.2019.1655101
https://doi.org/10.1080/17461391.2019.1655101
https://doi.org/10.1016/j.jsams.2011.02.003
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0040
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0040
https://doi.org/10.1016/0013-4694\(88\)90169-1
https://doi.org/10.1016/0013-4694\(88\)90169-1
https://doi.org/10.1016/J.JSE.2011.04.035
https://doi.org/10.1016/J.JSE.2011.04.035
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0055
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0055
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0055
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0055
https://doi.org/10.1002/ca.20784
https://doi.org/10.1007/s00421-012-2498-2
https://doi.org/10.1007/s00421-012-2498-2
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0070
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0070
https://doi.org/10.1155/2019/6212039
https://doi.org/10.1016/J.ULTRASMEDBIO.2021.10.017
https://doi.org/10.1016/J.ULTRASMEDBIO.2021.10.017
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0085
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0085
https://doi.org/10.1097/00003086-199609000-00002
https://doi.org/10.1097/00003086-199609000-00002
https://doi.org/10.1007/S00421-015-3214-9
https://doi.org/10.1123/ijspp.5.3.328
https://doi.org/10.1123/ijspp.5.3.328
https://doi.org/10.1152/physrev.00035.2013
https://doi.org/10.1016/j.jesf.2017.06.003
https://doi.org/10.1016/j.jesf.2017.06.003
https://doi.org/10.1016/j.jcm.2016.02.012
https://doi.org/10.1016/j.jcm.2016.02.012
https://doi.org/10.1080/17461391.2015.1022605
https://doi.org/10.5216/rpp.v23.54690
https://doi.org/10.1016/J.JELEKIN.2020.102509
https://doi.org/10.1016/J.JELEKIN.2020.102509
https://doi.org/10.1016/J.JELEKIN.2019.03.002
https://doi.org/10.1016/J.JELEKIN.2019.03.002
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0140
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0140
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0140
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0145
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0145
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0145
https://doi.org/10.1519/JSC.0000000000003033
https://doi.org/10.1371/JOURNAL.PONE.0218209
https://doi.org/10.1016/1050-6411\(94\)90017-5
https://doi.org/10.1152/AJPREGU.1995.269.3.R536
https://doi.org/10.3390/IJERPH17197339
https://doi.org/10.1515/hukin-2017-0047
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0180
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0180
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0180
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0180
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0180
https://doi.org/10.1016/J.JELEKIN.2008.04.013
https://doi.org/10.1093/ptj/46.10.1043
https://doi.org/10.1519/JSC.0B013E3181DDFAE7
https://doi.org/10.1519/JSC.0B013E3181DDFAE7
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0200
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0200
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0200
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0200
https://doi.org/10.3389/fphys.2017.00985
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0210
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0210
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0210
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0215
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0215
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0215
http://refhub.elsevier.com/S1050-6411\(22\)00095-5/h0215
https://doi.org/10.1249/MSS.0B013E3182995349
https://doi.org/10.1016/J.JELEKIN.2011.11.004
Journal of Electromyography and Kinesiology 67 (2022) 102722
10
Wickham, J.B., Brown, J.M.M., 2012. The function of neuromuscular compartments in 
human shoulder muscles. J Neurophysiol. 107, 336–345. https://doi.org/10.1152/ 
jn.00049.2011. 
Yasuda, T., Fujita, S., Ogasawara, R., Sato, Y., Abe, T., 2010. Effects oflow-intensity 
bench press training with restricted arm muscle blood flow on chest muscle 
hypertrophy: a pilot study. Clin Physiol Funct Imaging. 30, 338–343. https://doi. 
org/10.1111/J.1475-097X.2010.00949.X. 
Zabaleta-Korta, A., Fernández-Peña, E., Santos-Concejero, J., 2020. Regional 
Hypertrophy, the Inhomogeneous Muscle Growth: A Systematic Review. Strength 
Cond J. 42, 94–101. https://doi.org/10.1519/SSC.0000000000000574. 
J.C.S. Albarello et al. 
Conteúdo licenciado para Ivna -
https://doi.org/10.1152/jn.00049.2011
https://doi.org/10.1152/jn.00049.2011
https://doi.org/10.1111/J.1475-097X.2010.00949.X
https://doi.org/10.1111/J.1475-097X.2010.00949.X
https://doi.org/10.1519/SSC.0000000000000574