Longer repetition duration increases muscle activation and blood lactate response in matched resistance training protocols

–This study analyzed the effect of different repetition durations on electromyographic and blood lactate responses of the bench press exercise. Fifteen recreationally trained male volunteers completed two training protocols, matched for intensity (% one-repetition maximum; 1RM), number of sets, number of repetitions, and rest intervals. One of the protocols was performed with a repetition duration of 4 s (2 s concentric: 2 s eccentric; 2:2 protocol), whereas the second protocol had a repetition duration of 6 s (2 s concentric: 4 s eccentric; 2:4 protocol). The results showed higher normalized integrated electromyography (pectoralis major and triceps brachii) for the 2:4 protocol. Blood lactate concentration was also higher in the 2:4 protocol across all sets. These results show that adding 2 s to the eccentric action in matched training protocols increases muscle activation and blood lactate response, which reinforces the notion that increasing repetition duration is an alternative load progression in resistance training.


Introduction
Repetition duration, defined as the time spent performing the concentric and eccentric muscle actions during a repetition, should be considered when prescribing a resistance training program (American College of Sports Medicine [ACSM], 2009; Bird, Tarpenning, & Marino, 2005).Repetition durations between 4 s and 6 s are recommended for resistance training emphasizing muscle hypertrophy (ACSM, 2009;Wernbom, Augustsson, & Thomeé, 2007) and are commonly used by weight trainers (Headley et al., 2011).However, comparative physiological data about the effect of these durations on resistance training are scarce.
Although it is expected that the increase in exercise time could result in a rise in electromyographic amplitude (Hunter et al., 2004), studies that examined the effect of repetition duration in muscle activation have shown different results.While Burd et al. (2012) verified higher concentric electromyographic amplitude when performing longer duration exercise (12 s vs. 2 s), Sampson et al. (2014) found no differences on the tested situations (maximum speed, ~3 s, and 4 s) for this same type of muscle action.Unlike these studies, Sakamoto and Sinclair (2012) verified an increase in concentric muscle activation when using shorter repetition durations (maximum speed, 1.9 s, 2.8 s, and 5.6 s).Furthermore, in the studies of Sampson et al. (2014) and Sakamoto & Sinclair (2012) the analysis of multiple sets was not carried out, neither the protocols were equalized by training volume (number of repetitions), training load component that affect deeply the degree of muscle activation (Lacerda et al., 2016;Yue, Alexander, Laidlaw, Gmitro, Unger, & Enoka, 1994).The lack of control of the repetition duration and of the equalization of all variables of the training protocol, except the independent variable, has been a methodological problem in many studies involving the manipulation of the repetition duration on resistance training (González-Badillo, Rodríguez-Rosell, Sánchez-Medina, Gorostiaga, & Pareja-Blanco, 2014).
In addition to those controversial results, it should be highlighted that the protocols used by Burd et al. (2012), even though equalized by training volume, had quite different repetition duration values (Δ = 10 s), and are considered outside of the range suggested for muscle hypertrophy (ACSM, 2009;Bird et al., 2005;Schoenfeld, Ogborn, & Krieger, 2015;Wernbom et al., 2007).It can also be noted that the training protocols analyzed in the aforementioned study (Burd et al., 2012) had low intensity (30% of one repetition maximum -1RM).Considering that muscle activation response is affected by the intensity of training (%1RM) (Cook, Murphy, & Labarbera, 2013), and the fact that it has been identified in the literature the interaction between the intensity and repetition duration in the electromyographic amplitude (Sakamoto & Sinclair, 2012), further research is necessary to establish the effect of repetition duration on electromyographic responses during the execution of protocols with higher intensity.Therefore, to our knowledge, no studies have compared the effect of repetition duration on electromyographic response in matched protocols with multiple sets and repetition duration configuration that it has been recommended for muscle hypertrophy.Research data involving this issue may allow insights into other physiological responses considering matched protocols.Therefore, the purpose of the present study was to compare the effect of 4 s (2 s concentric:2 s eccentric; 2:2) and 6 s (2 s concentric:4 s eccentric; 2:4) repetition duration on muscle activation and blood lactate response using matched resistance training protocols.We hypothesized that the increase of the exercise time by manipulating the repetition duration would increase the amplitude of electromyographic signal.We also hypothesized that longer repetition duration would augment blood lactate concentration due to increased fast-twitch motor unit recruitment and consequently higher anaerobic glycolysis.

Participants
Fifteen male weight trainers (mean age 24.4 ± 4.4 years; mean height 1.77 ± 0.07 m; mean body mass 78.3 ± 9.4 kg; mean 1RM 93.4 ± 10.4 kg) participated in this study.The inclusion criteria for participation were (a) currently performing resistance training continuously for at least 6 months before the start of the study; (b) no functional limitations with regard to performing the 1RM test or the training protocols; and (c) the ability to lift a weight corresponding to their own body mass on the 1RM bench press exercise.The volunteers were informed about the study objectives, procedures and risks and freely signed an informed consent form.The local ethics committee of the university approved this study, which complies with international standards.The volunteers' training routines were modified during data collection, in order to avoid performing exercises that use the pectoralis major, anterior deltoid, or triceps brachii muscles 48 hours prior to sessions.Participants were also instructed to maintain the same dietary practices before each session.

Experimental design
This study used a crossover design to examine the effect of resistance training protocols differentiated by repetition duration (2:2 and 2:4) on electromyographic responses and blood lactate concentration.Each volunteer attended the laboratory on 4 different days (Experimental Sessions 1 through 4) separated by at least 48 hours.The registration of electromyographic activity occurred during the performance of each set of the training protocols, while blood samples for the estimation of the blood lactate were obtained before and after the sets.The same data collection schedule was maintained for each volunteer across all sessions.

Experimental session 1
After assessing the anthropometric measurements, the range of motion and the positions of the hands and head on the equipment were standardized.This standardization was carried out after each volunteer has been positioned as close as possible to his training routine in the bench press exercise and performed some repetitions without additional weight on the bar.Subsequently, the volunteers performed the 1RM test.The 1RM test was performed during the first session to familiarize the volunteers with the procedures.The test began with an eccentric muscle action by lowering the bar to the sternum, followed by a concentric muscle action, determined by the extension of the elbows.It was performed a maximum of 6 attempts, with 5 min rests and a minimum increase of 2 kg on each attempt.An average of 4.2 ± 1.0 attempts was necessary to determine the 1RM performance for experimental session 1.As the last procedure of experimental session 1, participants were also familiarized with the use of the metronome (60 beats/min) performing one of the training protocols to be implemented in experimental sessions 3 and 4.

Experimental session 2
The first procedure the experimental session 2 was the execution of the 1RM test, as previously described.The 1RM test was performed to determine the weight for the following sessions.An average of 3.9 ± 0.8 attempts was necessary to determine the 1RM performance for experimental session 2. After completion of the 1RM test, as well as in experimental session 1, participants were also familiarized with the use of the metronome performing the other training protocol to be implemented in experimental sessions 3 or 4.

Experimental sessions 3 and 4 Training protocols
In experimental sessions 3 and 4 the subjects were randomly submitted to the training protocols 2:2 and 2:4.The training protocols consisted of 3 sets, 6 repetitions and 3 min rests between sets at an intensity of 60% 1RM, with different repetition durations (2:2 or 2:4).These training protocols were determined in a previous study (Diniz, Martins-Costa, Machado, Lima, & Chagas, 2014), which verified that the volunteers could not complete the entire protocol for the greater repetition duration (2:4) using a greater number of sets, repetitions or intensity.Furthermore, we aimed to maintain the protocol configuration according to the recommendations for strength training for muscle hypertrophy (ACSM, 2009;Bird et al., 2005;Wernbom et al., 2007).

Procedures overview
An electrogoniometer was positioned on the volunteer's elbow, and electrodes were fixed to the pectoralis major and triceps brachii muscles as part of the first procedure in experimental sessions 3 and 4. The skin was marked using a semi-permanent pen to reposition the electrogoniometer and electrodes and the same researcher determined landmarks and carried out the positioning of equipment in both experimental sessions.The electrodes and the electrogoniometer were initially fixed, and the volunteers remained seated for 10 min; at this point, the first blood sample was collected to analyze the blood lactate concentration at rest.The remaining samples were collected 1 minute after each set of the training protocols.Electromyographic activity was recorded while performing each set of the training protocols.

Electrogoniometer
A calibrated electrogoniometer (Biovision, Wehrheim, Germany) was fixed on the right elbow of participants using double-sided adhesive tape and elastic bands.Once stored, the electrogoniometer raw data were converted into angular displacement data and filtered through a 4 th -order Butterworth low-pass filter with a cut-off frequency of 10 Hz.The duration of each repetition was calculated by the time between the points of lowest angular displacement (elbow extension) recorded by electrogoniometer during the execution of the training protocols.Additionally, the electrogoniometer was also used to determine the angular velocity and elbow range of motion.

Electromyography
The surface electromyography procedure (Biovision, Wehrheim, Germany) followed the recommendations of Hermens, Freriks, Disselhorst-Klug, and Rau (2000).Bipolar surface electrodes (Ag/AgCl) were placed parallel to the muscle fibers of the volunteers' right pectoralis major (sternal portion) and triceps brachii (long head portion) muscles.The skin area was shaved and cleaned with alcohol and cotton prior to placing the electrodes.The electrodes were placed in pairs, 2 cm apart from their centers at the point of greatest muscle belly.The ground electrode was fixed at the olecranon.The electromyographic data acquisition was amplified 500 times.After stored, these data were filtered (2 nd -order Butterworth band-pass filter of 20-500 Hz) and rectified to calculate the signal amplitude through the integrated electromyography (iEMG).The iEMG was calculated for the concentric muscle actions in each set and then divided by the respective time to analyze the electromyographic response during the training protocols (Ahtiainen & Hakkinen, 2009;Pincivero, Gandhi, Timmons, & Coelho, 2006).The mean concentric iEMG of the set was divided by the iEMG of the first repetition of each protocol performed (Ahtiainen & Hakkinen, 2009).Therefore, the mean set percentage values normalized by de first muscle action of the day were generated (mean normalized iEMG).The electrogoniometer was used to separate the muscle actions.The electromyographic and electrogoniometer signals were synchronized and converted using an A/D board (Biovision, Wehrheim, Germany) and sampled at a frequency of 2,000 Hz.Appropriate software (DasyLab 10.0, Measurement Computing, MA, USA) was used to record and treat the data.

Blood lactate concentration
Blood samples were collected from a puncture to volunteers' left earlobes using sterile, disposable lancets.The earlobe was cleaned with neutral soap and water and then sterilized with alcohol 70% before puncturing.A 30 μl sample of blood was collected into heparinized capillary tubes, which were transferred into other tubes containing 60 μl of 1% sodium fluoride and then stored in a refrigerator maintained at a temperature of -20º C. Subsequently, the samples were defrosted and analyzed in duplicates on the Yellow Springs Sport 1500 Lactate Analyzer device (Yellow Springs, OH, USA).

Data analyses
Distribution normality and homogeneity of variances were initially assessed using the Shapiro-Wilk and Levene's tests, respectively.The data were expressed as means and standard deviations, and the level of significance adopted for all analyses was P < 0.05.Logarithmic transformation of the normalized iEMG data was necessary to obtain a normal distribution or homogeneity of variances.The repeated-measures two-way ANOVA (training protocol x sets) was used for each muscle separately in the electromyographic analyses, as well as to compare lactate concentration.When necessary, a post hoc Tukey's test was used to identify the differences reported in the ANOVAs.Related-sample t-tests were used to compare repetition durations, ranges of motion, and angular velocities between protocols.Post hoc power analysis was performed for both ANOVA and t-test.The Intraclass Correlation Coefficient (ICC [3,1] ) of the concentric electromyographic activity found in the first repetition of Experimental Sessions 3 and 4 was calculated; these inter-session values were 0.85 for the triceps brachii and 0.93 for the pectoralis major.

Results
The main effects of protocol (F 1,14 = 5.69; P = 0.032; power = 0.60) and set (F 1,14 = 17.01;P < 0.001; power = 0.99) were significant for pectoralis major muscle activation.Our data show that the normalized iEMG in 2:4 protocol was higher than the 2:2 protocol, as well as the protocols increased the normalized iEMG throughout the sets.Post hoc comparisons indicated a progressive increase in muscle activation over the sets (Figure 1).No significant interaction was observed between protocol and set (F 2,28 = 1.37;P = 0.271; power = 0.17).The main effects of protocol (F 1,14 = 5.48; P = 0.034; power = 0.59) and set (F 1,14 = 10.66;P = 0.004; power = 0.94) were also significant for the triceps brachii muscle.Similarly, 2:4 protocol showed higher normalized iEMG than the 2:2 protocol, and the protocols increased the normalized iEMG throughout the sets.However, Tukey post hoc test found differences only when the 3 rd set is compared with the 1 st and 2 nd sets (Figure 2).No significant interaction was observed between protocol and set (F 2,28 = 1.53;P = 0.234; power = 0.19).
The main effects of protocol and set were significant with regard to blood lactate concentration.In addition, a significant interaction effect was observed between protocol and set (F 3,42 = 46.59;P < 0.001; power = 1.00).Figure 3 shows the blood lactate concentrations for the different training protocols.These results indicate that blood lactate concentrations increased for both protocols throughout the sets, and blood lactate concentration was higher in the 2:4 protocol than the 2:2 protocol for all sets, except during rest measurement.

Discussion
This study examined whether longer repetition duration (2:2 vs. 2:4) would result in greater electromyographic responses and higher blood lactate concentrations in matched training protocols.The results showed that normalized iEMG response for concentric actions was greater in the 2:4 protocol than in the 2:2 protocol for the pectoralis major and triceps brachii muscles.Furthermore, normalized iEMG response increased throughout the sets for both protocols.Blood lactate concentration was higher with longer repetition duration and increased throughout all sets.
In the present study, a higher normalized iEMG response in concentric muscle actions indicated that an increase in muscle activation was necessary to maintain the level of force necessary to complete the 2:4 protocol.Considering that the training protocols were matched, this result may be attributed to a longer duration of eccentric muscle action in the 2:4 protocol when compared to the 2:2 protocol.This longer duration denotes a decreased movement velocity during eccentric action, which has been linked to a decreased use of elastic energy in the stretch-shortening cycle (SSC) (Bosco, Komi, & Ito, 1981;Cronin, Mcnair, & Marshall, 2002).In addition, previous studies have shown that training protocols performed with longer duration of eccentric action caused an increase in eccentric-concentric transition time (Martins-Costa, Diniz, Machado, Lima, & Chagas, 2012;Sampson et al., 2014).Wilson, Elliott, and Wood (1991) showed that an increased transition time between eccentric and concentric actions (from 0.6 s to 1.27 s) resulted in lower impulse values early in the concentric muscle action following a decreased use of elastic energy, which reduced muscle force production.Thus, differences in transition time associated with the increase in the duration of the eccentric action in the 2:4 protocol might also have negatively affected the use of elastic energy.Given that the external resistance to overcome the concentric actions was the same in all repetitions for both protocols, it is possible that the participation of additional motor units was required in the 2:4 protocol to maintain strength performance during the concentric muscle action.Similar results were found by Burd et al. (2012).Although these authors analyzed different repetition durations (12 s vs. 2 s) of those compared in this study (4 s vs. 6 s), the longer duration used by Burd et al. (2012) also caused an increase in electromyographic amplitude, especially at the end of each set.Therefore, the data from the present study reinforce the expectation that an increase in the duration of muscle contraction at submaximal intensities can promote higher levels of muscle activation, a neuromuscular behavior also commonly seen in the electromyographic amplitude analysis of isometric sustained submaximal contractions (Hunter et al., 2004;Suzuki et al., 2002).As mentioned previously, this rise in the amplitude of electromyographic signal is at least in part an indicative of the occurrence of increased recruitment of motor units in an attempt to preserve the desired strength levels (Hunter et al., 2004), which in turn has been pointed out as an important neuromuscular response related to increased muscle strength and hypertrophy adaptation (Schoenfeld, 2013;Spiering et al., 2008).However, other factors, such as the increased firing frequency and synchronization of motor units, may also influence the electromyographic amplitude (Hunter et al., 2004;Suzuki et al., 2002).
In contrast, previous studies have reported different results (Sakamoto & Sinclair, 2012;Sampson et al. 2014).However, the studies of Sakamoto and Sinclair (2012) and Sampson et al. (2014) investigated one set of exercise to muscle failure, probably resulting in a non-equalized volume (number of repetitions) in each of the experimental conditions, so that the observed differences on electromyographic activity could not be mainly attributed to repetition duration.
The present investigation revealed also an increase in the electromyographic activity throughout the sets, findings observed in other studies (Smilios et al., 2010;Walker et al., 2011).As previously highlighted, participants should overcome the same external resistance for all repetitions.Thus, the increased electromyographic activity may reflect the insufficient rest interval for adequate recovery of some previously activated motor units, thereby demanding the participation of additional motor units in the next set.Mendez-Villanueva, Baudry, Riley, and Rudroff (2009) also suggested this mechanism after finding an increase in electromyographic activity across repeated isometric actions with a reduced pause for recovery.
Similarly to the electromyographic responses, blood lactate concentration increased along the sets in both protocols, result already seen in previous investigations (Lacerda et al., 2016;Smilios et al., 2010;Wirtz , Wahl, Kleinöder, & Mester, 2014).These data reinforce the expectation of high anaerobic demand required during the execution of each set of the resistance training protocols (Wirtz et al., 2014).With regard to the comparison of protocols, higher blood lactate concentration values were recorded in the 2:4 protocol compared with the 2:2 protocol, confirming data from previous studies that also equalized the training protocols (Mazzetti, Douglass, Yocum, & Harber, 2007).Given the higher normalized iEMG value found in the concentric muscle actions of the 2:4 protocol, additional motor units with higher glycolytic capacities were presumably recruited (Eckhardt et al., 2011;Takarada et al., 2000;Walker et al., 2011), which might promote an increase in blood lactate production compared with the 2:2 protocol.In contrast, Headley et al. (2011) found no difference in blood lactate concentration when comparing the protocols (4 s vs. 6 s), although the protocols performed were not matched by training volume, a training load component that also interfere with the blood lactate responses (Buitrago, Wirtz, Flenker, & Kleinöder, 2014;Lacerda et al., 2016).On other hand, in the study of González-Badillo et al. (2014) training protocols were equalized and higher lactate values were obtained at the end of the protocols of shorter repetition duration (higher repetition velocity).The authors explained this result by arguing that greater force production would be required to perform faster movements, which would also result in a greater recruitment of muscle fibers with higher glycolytic potential.
These controversial results may be related to the methodological differences, for example, the time under tension adopted in different studies.While in the research of González-Badillo et al. (2014) the approximate time under tension per set performed in the longer repetition duration protocol was 18 s, in the study of Mazzetti et al. (2007) the protocol of longer repetition duration resulted in 32 s.In the present study, time under tension was 36 s for the 2:4 protocol.Therefore, possibly the training loads imposed by longer repetition duration protocols adopted in current study, as well as in Mazzetti et al. (2007), have promoted greater degree of fatigue than the longer repetition duration protocol of the González-Badillo et al. (2014) study.Accordingly, greater recruitment of motor units may have occurred during exercise (Hunter et al., 2004), as well as increased blood lactate responses (Gladden, 2004).

Conclusion
This study revealed that longer repetition duration with similar concentric duration, but higher eccentric action duration, increases the blood lactate response and muscle activation.These findings indicate higher physiological demands with longer repetition duration.The relevance of this data is that increasing repetition duration should be considered as a progression in resistance training.

Figure 1 .
Figure 1.Mean normalized iEMG of the pectoralis major muscle for each training protocol (values normalized using the 1st repetition of the day).*Different from the 2:4 protocol (main effect); # Different from previous set (main effect); iEMG: integrated electromyographic signal.

Figure 2 .
Figure 2. Mean normalized iEMG of the triceps brachii muscle for each training protocol (values normalized using the 1st repetition of the day).*Differentfrom the 2:4 protocol (main effect); # Different from previous sets (main effect); iEMG: integrated electromyographic signal.

Figure 3 .
Figure 3. -Blood lactate concentration at rest and after each set with regard to the 2:2 and 2:4 protocols.