Squatting involves dynamic control of lower limb muscles, and it is widely used to emulate daily activities because of the coordinated interaction of muscle groups (38). Squats can also be performed as a screening tool or as knee and hip exercises to strengthen the thigh musculature (28,33). Its efficacy in increasing strength has been established (1,31,43). However, novel techniques to further improve its effectiveness are still being investigated. The adaptations been studied include changes in the depth of the squat (10,31,41), adding whole-body vibration (25), changing the torso position, the stance width (24), or adding external loads (10,41).
The compressive and shear forces in the knees (patellofemoral, tibiofemoral, and tibiofemoral joints) progressively increase as the knee flexes, reaching peak values near maximum knee flexion and having lower anterior shear forces between 0° and 60° of knee flexion (14). This is especially important in individuals with conditions that preclude heavy joint loading with impaired stability, including athletes recovering from injury, individuals with bone or joint conditions, and old adults with balance issues (32,37). These individuals are likely to benefit from a progressive exercise program (18) to strengthen lower limb muscles. Squats are considered a safe, functional, and effective closed chain activity (20) but are often prescribed late during the rehabilitation process with open chain exercises being prescribed earlier. However, functional exercises as squatting should be encouraged during early recovery process. In this sense, adding different types of stimuli to increase muscle activation during squat under more conservative ranges could improve efficiency while sustaining safety.
Pilates is a popular form of exercise for conditioning and rehabilitation (2,11), which includes concentration (attention to perform the exercises), centering (tightening of the abdominal muscles, lumbar multifidus, and pelvic floor muscles responsible for static and dynamic stabilization of the body using the drawing-in maneuver), control of posture and movement during the exercises, precision (accuracy of exercise technique), flow (smooth movement transition), and coordinated breathing (44). Pilates is frequently prescribed to people with low back pain due to its focus on activating stabilizing muscles of the trunk and lower back (34,36). Despite the frequent prescription of Pilates to manage low back pain, its principles may affect other body segments (8). A study compared abdominal curl exercises with and without using the Pilates breathing technique and found greater abdominal muscle activation during with Pilates breathing (5).
Greater activation of lower limb muscles increases joint stability, force ratio (16,17), and motor unit recruitment (17,39). However, no study assessed if performing squats while doing the drawing-in maneuver with and without the Pilates breathing technique affects the activation of lower limb muscles. If Pilates breathing associated or not with a drawing-in maneuver during squats increases lower limb muscle activation patterns during squats, the combination could be used to improve squat exercise efficiency within conservative ranges to be prescribed earlier in the rehab process. Therefore, the purpose of this study was to assess the activity of lower limb muscles during squat with and without abdominal drawing-in and Pilates breathing. The hypothesis was that lower limb muscle activation during squats would be higher with abdominal drawing-in and Pilates breathing.
Experimental Approach to the Problem
A descriptive, repeated measures design was used to compare the activation of the lower limb muscles (dependent variables) among conditions and between phases (independent variables) during squats. We compared squats performed by subjects under the following conditions in a randomized order using the online tool https://www.randomizer.org/: (I) normal breathing, (II) drawing-in maneuver with normal breathing, and (III) drawing-in maneuver with Pilates breathing.
The sample size was calculated using the G-POWER software (Version 3.1.5, Franz Faul, Universitat Kiel, Germany) considering an effect size of 0.85 (8) and an alpha level of 0.05. The power analysis returned an actual power of 0.87 for a sample size of 12 subjects. A total of 20 young adults were recruited from Pilates course attendees and 13 women (22 ± 3 years old, range = 19–22 years; BMI = 23 ± 2 kg·m−2) agreed to participate. The local ethics committee for human investigation approved the procedures used in the study (protocol number 570.801), and subjects were notified of the benefits and potential risks involved before signing an informed consent form.
The inclusion criterion was to have completed the 2-week Pilates course and 3 Pilates sessions over a week period. During the first 2 sessions of Pilates, the emphasis is on activating the deep abdominal muscles associated with the breathing technique. To be eligible, the volunteers could not be engaged in regular exercise programs during the previous year. They also had to be classified as “minimally active” or “inactive” using the short version of the International Physical Activity Questionnaire (27), so muscle adaptations were not biased because of training, masking the effect of breathing, and/or drawing-in maneuver on lower limb's muscle recruitment. In addition, the subjects were assessed by a physiotherapist, and subjects with any of the following were not eligible to participate: dynamic knee valgus, hip bone rotation, leg length discrepancy, self-reported pregnancy, diagnosis of ankylosing spondylitis, presence of neurological signs such as paresthesia and compromised tendons' reflexes (9).
Another assessment by a trained Pilates instructor verified the ability to perform the drawing-in maneuver using manual palpation at the TrA/IO site (5). All subjects were able to sustain the TrA/IO recruitment for at least 15 seconds.
All data were collected during morning (8:00–11:00 am) from July 9 to July 26, 2013. First, the volunteers were positioned in a predefined position with the feet shoulder width apart with the toes pointed slightly outwards and performed squats from full extension to 60° of knee flexion under each of the conditions after 2 familiarization trials. Knee flexion was initially measured using a universal goniometer (CARCI, São Paulo, SP, Brazil) and subsequently controlled by a mark on the parallel wall. The knee flexion and knee extension phases were set at 2 seconds also with 2 seconds between and it was controlled by the therapist using a chronometer (VL-501 Digital Chronometer; Vollo, Cotia, SP, Brazil). A verbal stimulus was given to start and end each flexion and extension phase (“go” and “stop”). For each condition, 3 trials were performed with a 3-minute rest period between trials.
During the normal breathing condition (I), the subjects were instructed to inhale during the knee flexion phase and exhale during the knee extension phase. During the drawing-in maneuver with normal breathing condition (II), the subjects were instructed to breathe the same way, but and also to perform and sustain the drawing-in maneuver during the squats to increase the abdominal pressure by pulling the abdominal walls inside by contracting the transverse abdominal and oblique abdominal muscles (29). During the drawing-in maneuver with Pilates breathing condition (III), the subjects were instructed to use the Pilates breathing technique associated with the drawing-in maneuver. The Pilates breathing technique consists in deeply exhaling through the mouth with the lips slightly pursed during the knee flexion and extension phases, and quickly inhaling through the nose between the phases. Standardized instructions and training were given to ensure that the pelvis was kept leveled and the trunk and the head were maintained in vertical alignment.
Data Collection Equipment and Analysis
A surface electromyographer (sEMG) with 8 analog channels and integrated software was used to collect and analyze the data (MIOTEC SUITE; Biomedical Equipment, Porto Alegre, RS, Brazil). Analog to digital conversion was performed by an A/D board with 14-bit resolution input range, sampling frequency of 2 kHz, common rejection module greater than 100 dB, signal noise ratio of less than 3 μV root mean square (RMS), and impedance of 109 ohms. The sEMG signals were recorded with surface Meditrace Ag/AgCl electrodes with a center-to-center distance of 2 cm. The electrodes were applied parallel to the underlying muscle fibers of the rectus femoris, biceps femoris, medial gastrocnemius, and tibialis anterior on the dominant lower limb. The electrodes were positioned according to surface electromyography for non-invasive assessment of muscles recommendations (http://seniam.org/sensor_location.htm). A reference electrode was placed on the left lateral humeral epicondyle. Before fixation, the skin was cleaned with 70% alcohol followed by exfoliation using a sand paper for skin and a second cleaning with alcohol.
The signals were synchronized using the MIOTEC SUITE software with a sagittal plane video recorded using a webcam (C615; Logitech, Hong Kong, China). The sEMG signals were amplified and filtered (Butterworth fourth order; 20–450 Hz bandpass filter), and the RMS of the data was windowed at 125 ms. All sEMG data were normalized to the 3 highest peaks, and the mean muscle activity was calculated from 2-second windows for each squat phase. A masked rater experienced with video motion analysis identified the squat phases at specific video frames on each participant's recording using the MIOTEC SUITE. The rater classified flexion and extension phases based on the frame of maximal knee flexion.
The Shapiro-Wilk test was used to test the Gaussian distribution of the data. Normality was accepted, and a 2-way analysis of variance was used to assess differences between phases and among conditions (with least significant difference t test as a post hoc), and interactions between conditions (I, II, and III) and phases (flexion and extension). The significance was set at p ≤ 0.05. All statistical analyses were performed using Predictive Analytics SoftWare 18.0 statistical software (SPSS Inc., Quarry Bay, Hong Kong, China).
None of the subjects reported pain or discomfort during the exercises. There was no significant interaction between conditions and phases. Table 1 shows the normalized sEMG mean and SDs during the flexion phase. Significant differences among the 3 conditions were noted during the flexion phase for the rectus femoris, biceps femoris, and tibialis anterior, but not for the gastrocnemius medialis. During the flexion phase of squats performed under condition III (drawing-in maneuver and breathing technique), the rectus femoris and the biceps femoris recruitment was significantly higher than during conditions I and II. The tibialis anterior activation during the flexion phase was significantly higher during conditions II and III compared with condition I.
Table 2 shows the normalized sEMG mean and SDs during the extension phase. Significant differences among the 3 conditions were noted during the extension phase for the gastrocnemius medialis, with increased activity during condition I compared with conditions II and III.
In relation to the comparisons between flexion vs. extension phases, the rectus and biceps femoris activity was higher during the extension phase under conditions I and II (p < 0.008). The tibialis anterior activity was higher during the flexion phase under all conditions (p < 0.003), and the medial gastrocnemius activity was higher during the extension phase in condition I (p = 0.01).
Squats performed with abdominal drawing-in and Pilates breathing resulted in increased rectus, biceps femoris, and tibialis anterior activity during the flexion phase of squats. These findings are important to be considered for exercise prescription. Doing 60° squats with abdominal drawing-in and Pilates breathing may be an effective and safe exercise to use during early phases of knee injury rehabilitation. A potential explanation for our findings is that the greater lower limb muscle recruitment when using the Pilates breathing technique and the drawing-in maneuver during squats happened because these combined activities increased awareness during the task (44). Some studies have found that increased lumbar muscle cocontraction to promote stability for limbs' movements (4,42). Pilates breathing uses similar stabilization techniques during exercises by encouraging cocontraction of core muscles, and the results (increased stabilization) seem to be similar for the lower limb muscles during squats. It has been suggested that reduced anterior tibial translation is associated with increased hamstring activation (15), and the ability to increase hamstring recruitment is linked to the level quadriceps activation during a deep squat (6). In addition, knee extensors act eccentrically to control and stop knee flexion during squats (35). Our findings include increased rectus and biceps femoris activity (cocontraction) during condition III, supporting the hypothesis of an interdependence of the anterior and posterior thigh musculature. In addition, we found increased tibialis anterior activation during the flexion phase in conditions II and III. This result disagrees with Pasquet et al. (30), who found no difference in the recruitment of the tibialis anterior during concentric and eccentric contractions, but found a significant difference in motor unit discharge rate. The tibialis anterior contracted during the knee flexion to help stabilize the ankle joint by cocontracting with the gastrocnemius (35), an increased muscle recruitment in conditions II and III compared I is likely to have occurred to increase joint stabilization through increased neural drive (3,13).
Similar to our findings, a study of deep loaded squats found a low level of gastrocnemius medialis activity during the knee flexion phase and high activity during the knee extension phase assisting knee extension synergistically with the biceps femoris (35). In our study, we did not find differences among the conditions during the flexion phase, but during the extension phase, the drawing-in maneuver, associated or not with the breathing technique (conditions II and III), resulted in decreased medial gastrocnemius activation compared with condition I. Our interpretation is that the medial gastrocnemius and rectus femoris have a combined action to assist knee extension and that the biceps femoris helps ensure stability and safety (35,41) even without increased medial gastrocnemius activation. As the biceps femoris and the rectus femoris presented large and similar levels of activation in all conditions during the extension phase, the medial gastrocnemius was not required to support the stability during conditions II and III.
Our findings may also be explained by the fact that limb movements are linked to purposeful respiratory control through an interaction between the activation of the respiratory system afferent signals and the excitability of motor cortex (12,19). Increased corticospinal excitability of finger muscles has been found during voluntary breathing suggesting breathing-associated activation of the cortical motor areas enhancing motor function (26). A study assessed the corticospinal excitability of the vastus lateralis during isometric contractions while performing different breathing techniques by recording motor-evoked potentials using sEMG during transcranial magnetic stimulation and found higher motor-evoked potentials during purposeful inhalation and exhalation compared with normal breathing (40). Therefore, it is possible that purposeful breathing drove the muscle recruitment patterns observed. The Pilates breathing requires deep breathing while keeping the abdomen pulled in by means of active contraction of the transverse abdominis and pelvic floor muscles (23), emphasizing the exhalation. This breathing technique was associated with greater activation of the majority of analyzed lower limb's muscles.
Pilates breathing increases the volume and oxygenation levels (7) and might be used to support any exercise program to provide the physiological environment for a better muscle recruitment. This is supported by our findings and by the findings of other studies (5,8). A recent study found increased deep abdominal muscle activation during abdominal exercises using the Pilates breathing technique compared with regular breathing (5).
A study compared the thickness of the transverse abdominal and internal oblique muscles based on ultrasound imaging, and the sEMG activity of the external oblique muscle in 33 healthy men while performing the drawing-in maneuver or a maximum exhalation. Maximum exhalation produced significant increased thickness and sEMG amplitude compared with the drawing-in maneuver (21). Another study observed a selective increase in abdominal muscles' recruitment during maximum exhalation while performing a bridge exercise, suggesting that these muscles may exhibit stronger contraction during exhalation (22). In this study, the exception was the medial gastrocnemius, which showed a decreased level of muscle activation during the combined technique compared with the normal condition. During the flexion, neither the drawing-in maneuver nor the combined technique showed influence in the gastrocnemius muscle activation. However, during the extension, the medial gastrocnemius displayed a greater activation during the normal condition. It is possible that the medial gastrocnemius displayed different mechanical strategies during the squat. Other muscles that exert function on the hip and knee need to be assessed to support these ideas.
Some limitations may be addressed in this study. The sample size calculation was performed to produce statistically significant findings, although the clinical implications of these data might be limited, because they are restricted to a young, healthy population. The squats were performed without external load and to 60° of knee flexion, which do not improve quadriceps strength, whereas deep and loaded squats do (6,38). Different knee angles would be explored in further researches. The exact time of day testing was not controlled, but the temperature was consistent during the entire experiment's range of time because of the weather characteristics of the city. Also, strength assessments were not obtained in this study, which could provide better rationale for the results in a long-term exercise program.
In conclusion, doing squats with abdominal drawing-in and Pilates breathing resulted in increased rectus, biceps femoris, and tibialis anterior activity during the flexion phase of squats increasing movement stability with similar levels of muscle recruitment for knee flexion and extension phases, except for the tibialis anterior. Further studies with different populations and different ranges of knee angles are needed to reinforce the use of the technique in rehabilitation and sports sciences.
The result of this study suggests an implement for lower limb muscle activation during a 60° squat only by performing the drawing-in maneuver combined to a coordinated breathing technique. Therefore individuals aiming to enhance the neuromuscular stress in the lower limb muscles could benefit from Pilates breathing technique and the drawing-in maneuver when performing the squat only by adding these 2 techniques during the squat. This information may assist coach and physical therapists in designing progressive training programs using these techniques as a progression, as a coordinated system of trunk-lower limb exercise, and where an implement on muscle recruitment may be considered without increasing the external load.
No funding was received for this work from any organization.
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