Participants

Sixteen volunteers (7 women and 9 men) participated in this study. The mean age ± standard deviation (SD), height, and body mass of women were 21.7 ± 2.2 years, 165.0 ± 2.8 cm, and 57.6 ± 7.8 kg, respectively. For men, the mean age, height, and body mass were 0.8 ± 1.7 years, 179.5 ± 9.6 cm, and 70.9 ± 10.2 kg, respectively. All volunteers were competitive athletes from various sports (track and field, handball, and soccer) with an average of 7.7 ± 3.6 hours training per week. None of them reported any lower limb injury or back pain in the last three months nor any specific hamstrings injury in the last two years. During the present experiment, participants were asked to maintain their regular physical activities and dietary intake. They were also advised to refrain from intensive activity at least during the two days prior to an experimental session. All volunteers were fully informed about the experimental procedure and purpose of the study. They read and signed an informed consent form. The study was conducted following the Declaration of Helsinki and received approval from the Ethics Committee for Research in STAPS (CERSTAPS IRB00012476-2022-15-03-166). The sample size (n = 15) was calculated a priori using G*Power (version 3.1.9.6) based on an effect size of 0.40, power of 0.9, and probability error of 0.05. The recruitment started April the 1^st 2022 and ended the June 30^th 2022.

Experimental design

This study was a cross-over, randomized, and single-blind trial. Blinding was used for data analyses and statistics (N.B.). The volunteers visited the laboratory on four occasions. The first visit was used as a familiarization for all tests, warm-up, and stretching procedures. Anthropometrics (height, body mass) and lower back and hamstrings flexibility (stand-and-reach test) were also evaluated. The subsequent three randomized experimental sessions were: passive warm-up followed by static stretching (PasSTA), passive warm-up followed by neurodynamic stretching (PasND) and control condition (CON) composed of active warm-up followed by static stretching (Fig 1). Participants were tested at three-time points during all experimental sessions: before (PRE), after warm-up (WARM), and after stretching procedures (STRETCH). Tests, focusing on the hamstring muscles, included: passive knee extension stretch until the maximal point of discomfort to evaluate range of motion, stiffness and viscoelasticity, two maximal voluntary isometric contractions (MVC) with electromyography analysis (EMG), lower back and hamstrings flexibility assessed by the stand-and-reach test, and subjective rating of perceived exertion (RPE). The passive stretch and MVCs were conducted on the right side. All experimental sessions were performed on the same day of the week, at the same hour of the day and separated by seven days. The temperature of the laboratory was controlled and was statistically similar between all sessions (21.7 ± 1.5 °C). Volunteers were free to drink water ad libitum.

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Fig 1. General experimental design.

https://doi.org/10.1371/journal.pone.0322582.g001

Conditioning activities

Tests

During the passive knee extension stretch, and MVCs, participants sat on the isokinetic dynamometer (System 5 Biodex Corporation, Shirley, NY, USA) as previously described [28]. Briefly, the left hip was maintained at a 100° angle, and the right hip was flexed at an angle of 45° between the right thigh and torso. The axis of the right knee (lateral condyle) was aligned with the axis of the dynamometer. Velcro straps were firmly attached distally on the volunteer’s right thigh, above the right ankle, and over the pelvis, trunk, and contralateral thigh. The torque and EMG signals of the long head of biceps femoris (BF) and semitendinosus (ST) muscles were recorded using a Biopac MP150 system and the associated software (AcqKnowledge 4.2 for MP systems, Biopac System, Santa Barbara, CA, USA). A 1-kHz sampling frequency was used. Two pairs of silver chloride surface electrodes were placed over the BF and ST muscles following SENIAM recommendations. The interelectrode distance was 2 cm (center to center) and the reference electrode was fixed to the right patella. Low impedance (<5 kΩ) of the skin-electrode interface was obtained by shaving, abrading with sandpaper, and cleansing with alcohol. The EMG signals were amplified with a bandwidth frequency ranging from 10 to 500 Hz (common mode rejection ratio = 110 dB, gain = 500), and the root mean square value (RMS) was calculated over 250 ms sliding windows.

The passive knee extension stretch was used to evaluate the maximal knee range of motion, stiffness and viscoelasticity. It was conducted starting from a 90° knee joint angle until the point of maximum discomfort. A slow angular velocity (5 °.s^-1) was used to avoid the stretch reflex [17]. The maximal stretched position was held for 90 seconds, and then the leg was passively released to the initial position. During the initial phase of the passive stretch, the maximal passive torque and torque-time area were evaluated as stiffness indexes. While the leg was held in the stretched position, we assessed the torque decrease, i.e., the difference between the greater and smaller torque values, as an index of viscoelasticity [29]. A constant angle procedure was used during each experimental session, i.e., the PRE-test maximal range of motion was also used during the WARM and STRETCH tests.

The two isometric knee flexion MVCs were performed at a 90° knee angle. Participants were instructed to contract maximally for 5 seconds with a rest interval of the 15 seconds between the two attempts. The maximal knee flexion torque and the corresponding RMS values for both muscles were recorded. The best contraction, determined by the highest torque, was used for data analysis.

The lower back and hamstrings flexibility was assessed by the stand-and-reach test. This test was chosen in order to have a test that could easily be applied in the real practice. Briefly, participants stood upright with their feet parallel, and then they were requested to bend forward as far as possible [30]. The upper limbs were fully extended (elbow, wrist, and fingers), and the maximum distance achieved was quantified using a flexometer (TK500, Takei scientific instruments, Niigata, Japan). This procedure was performed once at each time point.

Rating of perceived exertion (RPE) was evaluated after warm-up and stretching procedures using a 10-points visual analogic scale (with 1 corresponding to a very light exercise and 10 a very hard exercise) [31].

Statistical analyses

Values were expressed as mean ± standard deviation (SD). The normality and sphericity of the data were tested and confirmed by the Shapiro-Wilk and Mauchly’s tests. Then, a two-way analysis of variance (ANOVA) with repeated measurements was performed (Condition × Time) with a Greenhouse-Geisser correction applied in the case of non-sphericity. The condition factor was the three experimental conditions (PasSTA, PasND and CON), and the time was the PRE, WARM, and STRETCH (for RPE assessed only after WARM and STRETCH). The Bonferroni post-hoc test was conducted in case of main condition or time effects, or time × condition interaction. The partial eta squared (pη²) was calculated from ANOVA results, with values of 0.01, 0.06, and above 0.14 representing small, medium, and large differences, respectively. p < 0.05 was taken as the level of statistical significance for all comparisons. All statistical procedures were conducted using JASP (version 0.14, JASP Team 2020, University of Amsterdam, available free at https://jasp-stats.org/download/).

Effects of warm-up

The present study first revealed increases in stand-and-reach following both the passive and active warm-up strategies. Studies have previously reported the efficiency of passive strategies on range of motion using local hot packs or whole-body hot water baths [32,33]. Active warm-up strategies such as jogging, cycling and/or athletic drills have also shown effective for range of motion improvements [4,5,34]. These improvements have been suggested to be mediated via muscle or core temperature-related mechanisms [5,10,33] which would affect the neuromuscular system. Amongst these, stretching tolerance (pain perception) and changes in muscle passive properties (passive stiffness and viscosity) are the most likely mechanisms [5,10,35]. Our results partially refuted some of these mechanisms. Indeed, there were no significant changes in the passive torque, torque-time area, and viscoelasticity during the passive knee extension stretch test. However, these findings partly supported previous studies [32]. In a similar study comparing passive and active warm-up strategies, authors found an increase in range of motion without any alteration of passive muscle properties [32]. Accordingly, these authors concluded that the gains in range of motion were primarily due to an increase in stretch tolerance as evidenced by higher passive torque for greater range of motion. While our study utilized a constant-angle procedure for measuring passive properties, our results support the likely role of stretch tolerance in increasing flexibility.

Warm-up, whether it is conducted with passive [36] or active strategies [10,27], are generally associated with improvements of the contractile function. Several mechanisms are implied such as calcium kinetics or muscle fluids [36]. In the present study, the contractile function was measured via a maximal voluntary contraction. No statistical differences were obtained for the maximal torque or corresponding EMG activity. These controversial results under passive conditions could firstly be attributed to the technical procedures used for warm-up. Studies generally employed hot-water immersions. Although, a hot room, specifically a sauna, was used here, the temperature applied (45 °C) falls within the temperature ranges generally recommended (for safety or tolerance) [36]. In contrast, the 20 minutes heat administration was shorter than many other studies. For example, some research observed improved contractile function following 90 minutes immersion in hot-water [37]. It is reasonable to speculate that a longer heat administration would have increased force production capacity. However, one can question the applicability of such long durations in sports settings.

The lack of increase in contractile function after active warm-up can secondly be explained by several main hypotheses. The contractile function was evaluated using maximal voluntary isometric contractions. However, this condition was not included in our warm-up set-up. The well-known specificity of warm-up effects (related to motor learning) should therefore be respected to observe positive effects after a comprehensive warm-up [27]. Finally, the test and data analyses could also explain the lack of contractile function enhancement. Applying different tests (such as a direct measurement of the rate of force development) or other analyses might be of interest [7,36]. Indeed, temperature-dependent effects appeared to be more effective on fast contractions [37]. However, one should acknowledge the lack of the skin or muscle temperature control. Indeed, it would have been useful to control the likely alterations in muscle temperature after both warming procedures and stretching.

Stretching effects

After passive or active warm-up, 6 sets of 30 seconds of static or neurodynamic stretching were applied. In contrast to our a priori hypothesis, an exacerbated increase in flexibility was observed for both stretching modalities. Such finding is partly in contradiction with previous studies [34]. Indeed, these authors concluded that 3 sets of 10 seconds stretching within a full, dynamic warm-up had no effect on flexibility. Accordingly, the conflicting findings might be related to the duration proposed for stretching. Although a short-volume of static stretching may slightly enhance flexibility, it has been reported that flexibility improvements from high-volume is better than short-volume of static stretching [38]. Indeed, authors did not exclude the possibility that adding longer static stretching periods instead of short ones to an active and full warm-up could enhance flexibility [39].

However, as for warm-up effects, this increase in flexibility was not associated with alterations in most muscle passive properties. This result could appear surprising since numerous studies have registered changes in muscle-tendon unit stiffness and viscosity after similar duration stretches [17,28,40]. However, changes in passive torque may not always be detected and could be influenced by the stretching technique and by measurements of passive properties. For instance, the impact of stretching on passive torque is typically observed during the final degrees of a passive stretch procedure [18]. The constant-angle procedure utilized in our study might obscure such changes. Furthermore, there was a large effect size on passive torque that approached statistical significance. It is probable that incorporating more participants or employing an alternative procedure would have revealed alterations in passive properties.

In contrast, the neural drive, witnessed by the ST RMS, was impaired after both stretching modalities. These results therefore suggested that conducting moderate duration stretching in association with a comprehensive warm-up was inefficient for subsequent performance [4]. Such results are commonly obtained in the literature [14,15,41] and point towards numerous central or peripheral origins that are regularly explored in research studies. However, despite the decrease in ST RMS, no associated alteration of the maximal voluntary torque was observed. Such finding is in contradiction with most of the literature concluding that prolonged stretching significantly impaired the maximal torque production capacity [14–16,38]. One should remember that both women and men were included in this study. It will inherently conduct to large maximal voluntary torque variability that can mask a potential time effect.

Interestingly, no difference was observed between static and neurodynamic nerve gliding procedures. This result suggested that these two stretching procedures could be used interchangeably for flexibility increases. However, both stretching procedures imply different mechanisms since different tissues are involved. While static stretching mostly alters the neuromuscular and muscle-tendon systems [17,40] neurodynamic procedures additionally affect nerves stiffness [42]. A decrease in nerve stiffness has been registered immediately after neurodynamic stretches [42]. However, the exact effects of neurodynamic techniques (whether using sliding or tensioning) need further studies to better determine the subsequent effects and mechanisms.

Limitation and perspectives

The present study has several limitations that should be acknowledged. As previously stated, the skin or muscle temperature has not been controlled. In addition, the stand-and-reach test was used as a flexibility measurement. The rationale for using this test is questionable since it involved both the lower back and hamstring muscles while stretching only engaged hamstring muscles. The conclusions obtained during this flexibility test and the passive knee extension test should therefore be compared with caution. However, these muscles were involved in our active and passive warm-up routines, which corresponded to the primary aim of our study. Finally, a moderate stretch duration, generally not recommended during warm-ups, was used here. Such rather long stretch duration was chosen to exacerbate stretching effects since less in known in the literature for the neurodynamic nerve gliding stretching modality.

Beside these limitations, the present study provided important practical applications for athletes. Firstly, passive strategies could be applied within warm-up routines. In addition to the gain in flexibility, passive warm-up has multiple interesting advantages for instance while reducing energy consumption. RPE was largely reduced with passive procedure as compared to active ones. Moreover, passive strategies permit to gain time during the whole pre-activity routine for instance to conduct concomitant mental tasks, such as mental imagery. Secondly, both warm-up strategies and stretching induced the same effects on muscle flexibility and strength. Although different neuromuscular mechanisms are likely involved, these various techniques can be used interchangeably to mitigate training monotony. However, both stretching modalities further increase flexibility but may impair subsequent muscle performance. Therefore, practitioners should prescribe stretching exercises based on the specific sport, event, and key performance indicators. Further studies should be conducted to better determine neuromuscular mechanisms and assess the utility of neurodynamic techniques in sports science.