Introduction
A variety of warm-up methods have been used before physical exercise to reduce the risk of injuries and to enhance performance on the subsequent main activity (5,26,27 ). In this respect, some authors suggest that these warm-ups can involve general activities, specific warm-ups, and different stretching methods (1 ). General warm-ups consist of low-intensity aerobic activities, such as running or cycling, with the aim of increasing muscle temperature and neuromuscular function (1,2 ).
Specific warm-ups (SWs) include exercises that are similar to the main activity, with a progressively increasing intensity, to enhance the neuromuscular activation system. A SW added to a general warm-up for a 1 repetition maximum (1RM) test in leg press showed an improvement of 8.4% (1 ). Recently, it was demonstrated that a SW resulted in higher number of maximal repetitions for the subsequent lower limb strength training session (STS) than ballistic and passive static stretching (PSS) methods (25 ).
Some stretching methods can also be considered as a warm-up (1 ). The duration of the stretching stimulus performed before the main activity is directly related to the performance (3 ). The effects of stretching methods as warm-ups previous to a strength performance have been studied in relation to the number of repetitions (3,11,12 ), 1RM tests (2,4 ), vertical jump (6 ), and isometric strength (21 ). Passive static stretching (4,6,21 ), proprioceptive neuromuscular facilitation (PNF) (3,6,14 ), and SW (1,11 ) have been manipulated according to The American College of Sports Medicine's recommendations (13 ). However, controversial results can still be found as the intervals amplitudes for duration, intensity, and number of sets allow different protocols.
Overall, there is a reduction in strength levels after stretching protocols (10,14,27,28 ). This decrease has been explained by 2 main mechanisms. The first is related to the reduction in neural activation in response to the stimulus given to the Golgi tendon organ (10 ). The second mechanism refers to changes in the mechanical properties of the muscle-tendon unit (15 ). In this case, the tendon tension during stretching would alter its viscoelasticity, causing a stress relaxation behavior that reduces tendon stiffness and affects the force transmitted by the muscles (14 ).
Additionally, the arrangement of the muscle fibers is directly related to muscle force generation (16,18 ). Changes in the muscle architecture after acute stretching have been reported, such as a decrease in the pennation angle (PA) and an increase in the fascicle length (FL) (23,24 ). The way in which such transient architectural rearrangement could influence the shortly after force production is still unclear. As suggested on meta-analysis (27 ), there is inversely proportional relationship between muscle tendon compilancy and the efficiency force transmission (29 ).
Therefore, the purpose of this study was to investigate the acute effects of 2 stretching methods, PNF and PSS, and of a SW on the STS (number of repetitions of 4 exercises). Muscle architecture of the thigh muscles had been monitored before and after the stretching and SW. Based on the literature, the initial hypothesis is that the SW will result in performance improvements compared with stretching methods.
Methods
Experimental Approach to the Problem
This study was designed to investigate the effects of a SW and 2 different stretching methods (PNF and PSS) on strength performance. Muscle architecture using ultrasound (US) images of the vastus lateralis (VL) and biceps femoris (BF) muscles was monitored using 3 moments of the protocol. Nine subjects visited the laboratory 7 times with a minimum of 48 hours between the visits. The familiarization with the stretching methods and exercises was performed on the first visit. The subjects performed the strength test and were retested on the second and third days, respectively. From the fourth to the seventh day, the subjects were randomly selected to perform one of the 4 possible situations (PNF, PSS, SW, and CS). For these 4 visits, the subjects lay down on a stretcher for 10 minutes of rest before the US images were collected. Just after US acquisition, the subjects underwent intervention with one of the proposed methods (SW, PNF, or PSS), and immediately afterward, the US images were collected again. After this procedure, the following 4 exercises were executed in this order: leg extension, leg curl, leg press, and hack machine squat.
Subjects
Nine male volunteers (age: 24.81 ± 2.98 years, weight: 81.33 ± 11.46 kg, height: 1.77 ± 0.07 cm, and body mass index 25.81 ± 3.20 kg·m−2 ) participated in 4 different, randomly chosen experimental conditions. All subjects were involved in other recreational physical activities such as cycling, running, and swimming, but none of them had been strength training for the past 6 months. Thus, these subjects were considered untrained in strength training . Before data collection, the volunteers signed a free and informed consent form prepared according to Resolution 196/96 of the National Health Council. The subjects answered the Physical Activity Readline Questionnaire (PAR-Q) questionnaire and a general questionnaire designed to exclude individuals with possible cardiopulmonary or musculoskeletal diseases and user ergogenic substances. The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of the University Hospital, Federal University of Rio de Janeiro. Subjects were informed about the test procedures with the possible risks and benefits of the study. They signed an informed consent form before the tests began. No subject withdrew from the study.
Procedures
During the first visit, the subjects were familiarized to the 2 stretching methods and exercises, with a submaximal load, and 8 repetitions were performed. During the second and third visits, the subjects were initially placed in a supine position with their lower limbs relaxed for 10 minutes. The US images of the VL and BF of the dominant leg muscles were obtained immediately before and after the 8RM test and retest for each exercise (leg extension, leg curl, leg press and hack machine squat) performed according to the literature (14 ). A 10-minute interval was used among the 4 exercises of the 8RM tests that were applied in the same order.
In the fourth to seventh visits, the subjects initially remained in the supine position on a paddle with relaxed lower limbs for 10 minutes. Afterward, ultrasound images of the VL and BF (M01 —time point 1) were acquired for the dominant leg. Then, one of the 3 experimental protocols was randomly performed (PNF, PSS, and SW). A fourth control condition was also included (CS) where the subjects rest at the same initial supine position for similar intervals of time stretching PSS and PNF (3 minutes).
Immediately after the experimental protocols, the subjects returned to the stretcher for the STS procedure (M02 —time point 2). Afterward, the participants performed the STS with the following 4 exercises: leg extension, leg curl, leg press, and hack machine squat (Rotech Equipment, Goiania, Brazil). The 4 exercises were performed with limited 90° knee joint range of motion. The subjects were encouraged to perform as many repetitions as possible until there was concentric failure in the 3 sets of each exercise. The rest time between sets and between exercises was 90 seconds for all protocols (8 ). After the training session, the US procedure was repeated after the subjects rested for an additional 10 minutes with relaxed legs (M03 —time point 3).
The subjects were individually tested at the same time in the morning, and they were instructed to maintain nutrition habits during the experimental period.
Protocols for Stretching and Specific Warm-up
The PSS method involved 3 sets for flexor and knee extensor postures with 30-second intervals (Figure 1 ). The maximal joint amplitude was assisted reached, according to the subject's limit of discomfort, for 30 seconds (13 ). For the PNF stretching method, 3 series of the same knee flexor and extensor postures were performed (Figure 2 ). Immediately after reaching the maximal amplitude, the subjects were asked to isometrically contract the agonists for 6 seconds and then to relax when further amplitude was assisted reached and sustained for more than 24 seconds. Both methods of stretching exercises were performed with the same overall execution time.
Figure 1.: Passive static stretching and proprioceptive neuromuscular facilitation stretching of the hamstrings of the thigh muscles.
Figure 2.: Passive static stretching and proprioceptive neuromuscular facilitation stretching of the quadriceps of the thigh muscles.
For the SW, 20 repetitions of each exercise were performed, for 30 seconds, at a 30% 8RM load, with an interval of 30 seconds.
Ultrasound Procedures
The US images were acquired 4 times during the fourth to seventh visits, with an EUB-405 (Hitachi, Tokyo, Japan) with an 8-cm linear probe with a central frequency of 7.5 MHz with the aid of a gel for acoustic coupling (Ultrex; Farmativa Indústria e Comércio Ltda, Rio de Janeiro, RJ, Brazil).
The volunteers rested in the supine position on a stretcher. Longitudinal US images of the VL and BF muscles were acquired at 50% of the thigh length (19 ) of the dominant leg by an experienced examiner. Two images were consecutively acquired. Image processing and architectural muscle parameter measurements were blindly performed using a homemade routine (LabVIEW; National Instruments Corporation, Austin, TX, USA). One of the 2 images was considered for the analysis and was selected for having the best visual definition of the fascicles. Images from the second and third visits were used for reliability procedure. The PA was determined as the acute angle between the deep aponeurosis and the selected muscle fascicle. The fascicle length (FL) was determined as the length between the superficial and deep aponeuroses (Figure 2 ). These US architectural parameter (PA and FL) measures were already validated from cadaveric measurements (9 ).
Statistical Analyses
To estimate the architecture measurement reliability, the intraclass correlation coefficient (ICCr), coefficient of variation (CV, %), and confidence interval (CI) were calculated between the FL and PA measurements of the images of the first 2 days. The reliability for the FL and PA was considered high for the BF (ICCr = 0.922, CV = 4.11%, and CI = 0.607–0.997; and ICCr = 0.932, CV = 2.34%, and CI = 0.676–0.985, for FL and PA, respectively) and for the VL (ICCr = 0.920, CV = 8.13%, CI = 0.654–0.982; and ICCr = 0.964, CV = 2.56%, and CI = 0.843–0.997, for FL and PA, respectively).
After confirming the normal distribution using the Shapiro-Wilk test and calculating the 95% CI, ANOVA with repeated measures on the second factor (4 × 3) was applied to compare the 4 experimental pre-STS conditions at the 3 US measurement moments for the muscle architecture parameters.
Similarly, ANOVA was applied with 2 factors (4 × 4) to compare the training volumes in each exercise. A post-hoc Fischer least significant difference was applied with a significance level of p ≤ 0.05. We performed the analysis using Statistica software (Statsoft, Inc., Tulsa, OK, USA).
Results
The main results of the present study are related to the influence of the type of warm-up on the number of repetitions for each exercise (F(9,144) = 3.719, Figure 3 ). For all exercises, the PNF stretching method reduced the number of repetitions compared with SW and PSS. The significance levels for the leg extension exercise were p = 0.017 and p = 0.031 for SW and PSS, respectively. For the leg curl exercise, the PNF resulted in a lower number of repetitions than the CSs (p = 0.020, p = 0.001, and p = 0.006 for PSS, SW, and CS, respectively). For the leg press exercise, the significance levels from PNF to SW and to PSS were p = 0.031 and p = 0.001, respectively. In this exercise, PSS and SW resulted in a higher number of repetitions than the CSs (p = 0.005 and p = 0.001, respectively). For the hack machine squat, PSS resulted in a higher number of repetitions than the other 3 (p = 0.002 for PNF, p = 0.008 for CSs, and p < 0.001 for SW). Specific warm-up resulted in a higher number of repetitions than PNF (p < 0.001) and CSs (p < 0.001).
Figure 3.: Ultrasound image of the vastus lateralis muscle for pennation angle and fascicle length measurements.
The BF muscle showed a higher PA 10 minutes after the STS for the PSS method (Table 1 ) (M01 vs. M03 , p = 0.008); the FL increases immediately after PSS (p = 0.013) then decreases 10 minutes after the STS for the PSS method (p = 0.005) (Table 2 ). The VL muscle FL increases after STS for the PNF method (p = 0.039) (Table 2 ).
Table 1.: Pennation angle mean (degrees) and SD s for the vastus lateralis (VL) and biceps femoris (BF) at each measure moment (M01 , M02 , and M03 ).*
Table 2.: Fascicle length mean (centimeter) and SD s for the vastus lateralis (VL) and biceps femoris (BF) at each measure moment (M01 , M02 , and M03 ).*
Discussion
The aim of this study was to verify the impact of PNF and PSS methods and of SW on a subsequent strength session for lower limbs . The main findings were that the PNF stretching method caused an overall reduction in performance compared with the PSS method, SW, and CS. Additionally, the PSS method and SW showed an improvement in the number of repetitions for multijoint exercises. Specific warm-up showed no significant effects on the muscle architecture, which means that muscle fiber arrangements could not be responsible for these differences. For PSS, the FL and PA of the BF presented statistical changes and for PNF, the statistical variations were observed only on FL for BF.
We found a significant reduction in the number of repetitions of leg extension exercises after PNF stretching compared with the CS and static stretching (Figure 4 ). This was also described by others (14 ) who reported a decrease of approximately 2–3 maximal repetitions for leg extension exercises (80% 1RM) compared with the no stretching condition. A decrease in neural activation by Golgi Tendon Organs (GTO) agonist inhibition is the physiological mechanism commonly attributed to this fact (10 ). The GTO is an autogenic inhibition reflex discharged when high tension is detected in the tendon structure. With intense stretching, the muscle tension can discharge this reflex causing muscle inhibition, potentially protecting it from injuries (10 ). On PNF stretching, a large tension is generated enabling the Golgi reflex discharge leading to further muscle elongation in the next stretching phase. However, it was shown that although the inhibitory effects are temporary, the peak passive plantar-flexion torque was still reduced for about 1 hour (10 ). These authors suggested that the lasting of peak torque reduction could be attributed to biomechanical effects (10 ). The decrease in stiffness after intense stretching has been reported by others for the gastrocnemius and quadriceps muscles (7,17,20 ), whereas less force is transmitted to the skeleton by a more complacent structure.
Figure 4.: Representative graph of the number of repetitions for each exercise and group. For p ≤ 0.05, (A) differences for the proprioceptive neuromuscular facilitation ; (B) differences to the control; (C) difference between passive static stretching and specific warm-up.
Conversely, improvements for all exercises were recorded after PSS and SW. In relation to SW, this finding is in agreement with our previous study (25 ), where it was found an improvement in all exercises after a SW compared stretching protocols. As far as we know, no other study verified the effect of SW in STSs. Although we did not measure body temperature, some authors recommend 5–10 minutes of warm-up before using a strength test protocol (22 ). In our case, SW involved 20 repititions for 30 seconds at a 30% 8RM load in each of the 4 exercises, which approximates this recommendation. A possible explanation for the improvement in performance would be an increasing muscle temperature, as suggested by Sa et al. (25 ) after verifying the positive effects of general warm-up and SW on vertical jump performance. They suggested that muscle temperature favorably affects muscle performance by reducing viscous resistance which, in turn, raises the oxidative reaction speed limits and/or increases the muscles' oxygen supply through greater vasodilatation. This mechanism can explain our results, as the exercises use the same energy path.
The improvements in performance observed after PSS in all exercises were less evident than were for SW. Commonly, there is a force reduction after a stretching maneuver; for example, decrease in leg press performance after passive stretching (2 ) has been reported, contrary to our results. This difference can be related to the stretching volume where 6 passive stretching postures with 3 sets each were conducted for the quadriceps and hamstrings with a total volume of 20 minutes. This high volume of stretching causes the same effects observed in PNF stretching. For the present study, only one exercise for quadriceps and hamstrings was used, with a total volume of 3 minutes, probably with similar benefits as the SW mentioned above.
With respect to muscle architecture, the PSS method resulted in significant changes in FL of the BF muscles, which could be linked to more complacent structures. Nevertheless, the number of repetitions for the leg curl exercise did not change (Figure 3 ). Overall, the higher number of repetitions after this protocol shows that this specific muscle architectural change had no negative impact on subsequent force exertion.
We conclude that a SW method as well as PSS should be prescribed before a STS, whereas the PNF stretching should not be recommended. The performance differences after the stretching methods cannot be explained by changes in muscle architecture parameters, as already discussed by Simic et al (27 ) on previous meta-analysis.
Practical Applications
Stretching exercises are commonly prescribed in training centers, gyms, and fitness clubs as part of a warm-up routine. The results of the present study suggest that a SW and static stretching are the best warm-up options for coaches and athletes to increase performance on total repetition number for lower limb resistance training sessions. Otherwise, we also suggest avoiding PNF stretching before a lower limb training session.
Acknowledgments
The authors gratefully acknowledge the Brazilian National Board for Scientific and Technological Development CNPq and Rio de Janeiro Research Foundation FAPERJ for financial support. Funder Organization: FAPERJ, CNPq.
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