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Journal of Strength and Conditioning Research Publish Ahead of Print

DOI: 10.1519/JSC.0000000000001877

R-373816

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ACTIVITY OF LOWER LIMB MUSCLES DURING SQUAT WITH AND WITHOUT

ABDOMINAL DRAWING-IN AND PILATES BREATHING

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Laboratory of Electromyography and Orthopedics - UFVJM
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ALEXANDRE C. BARBOSA1, FÁBIO M. MARTINS2, ANGÉLICA F. SILVA2, ANA C. COELHO2,

LEONARDO INTELANGELO3, AND EDGAR R. VIEIRA4

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1
Department of Physical Therapy, Federal University of Juiz de Fora, Governador
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Valadares, Brazil

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Department of Physical Therapy, Federal University of Jequitinhonha and Mucuri
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Valleys, Diamantina, Brazil

3
Department of Physical Therapy, University Institute of Gran Rosario, Rosario,

Argentina

4
Department of Physical Therapy, Florida International University, Miami, USA

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Correspondent author: Alexandre C. Barbosa. Avenida Dr. Raimundo Monteiro

Rezende, 330, Centro, Governador Valadares/MG – CEP 35010-177. Phone/Fax: +55

(33) 3301-1000. E-mail: alexwbarbosa@hotmail.com

Disclosure of funding: No funding was received for this work from any organization.

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ABSTRACT

The purpose of this study was to assess the effects of abdominal drawing-in and Pilates

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breathing on the activity of lower limb muscles during squats. Adults (n=13, 22±3 years

old) with some Pilates experience performed three 60° squats under each of the

following conditions in random order: I) Normal breathing, II) Drawing-in maneuver

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with normal breathing, and III) Drawing-in maneuver with Pilates breathing. Peak-

normalized sEMG of the rectus femoris, biceps femoris, gastrocnemius medialis and

tibialis anterior during the knee flexion and extension phases of squat exercises were

analyzed. There were significant differences among the conditions during the knee
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flexion phase for the rectus femoris (p=0.001), biceps femoris (p=0.038) and tibialis
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anterior (p=0.001), with increasing activation from conditions I to III. For the

gastrocnemius medialis, there were significant differences among the conditions during
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the knee extension phase (p=0.023) with increased activity under condition I. The rectus

and biceps femoris activity was higher during the extension vs flexion phase under

conditions I and II. The tibialis anterior activity was higher during the flexion compared

to the extension phase under all conditions, and the medial gastrocnemius activity was

higher during the extension phase under condition I. Doing squats with abdominal

drawing-in and Pilates breathing resulted in increased rectus, biceps femoris and tibialis

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anterior activity during the flexion phase, increasing movement stability during squat

exercises.

KEY WORDS: electromyography, rehabilitation, physical therapy

INTRODUCTION

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Squatting involves dynamic control of lower limb muscles, and it is widely used

to emulate daily activities due to the coordinated interaction of muscle groups (38).

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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 been investigated. The adaptations been studied include changes in the depth of
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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
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tibiofemoral joints) progressively increase as the knee flexes, reaching peak values near
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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
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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

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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)

that 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

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posture and movement during the exercises, precision (accuracy of exercise technique),

flow (smooth movement transition), and coordinated breathing (44). Pilates is

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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
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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).

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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
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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
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not to a drawing-in maneuver during squats increase 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.

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METHODS

Experimental Approach to the Problem

A descriptive, repeated measures design was used to compare activation of the

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lower limb muscles (dependent variable) among conditions and between phases

(independent variables) during squats. We compared squats performed by subjects

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under the following conditions in randomized order using the online tool

https://www.randomizer.org/:

I. Normal breathing,
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II. Drawing-in maneuver with normal breathing, and

III. Drawing-in maneuver with Pilates breathing.

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Subjects

The sample size was calculated using the G-POWER™ software (Version 3.1.5,
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Franz Faul, Universitat Kiel, Germany) considering an effect size of 0.85 (8) and an
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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 twenty young adults were recruited from Pilates course

attendees and 13 women (22±3 years old; IMC=23±2 kg/m2) agreed to participate. The

local ethics committee for human investigation approved the procedures employed in

the study (#570.801) and subjects were notified of the benefits and potential risks

involved prior to signing an informed consent form.

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The inclusion criterion was to have completed the two-week Pilates course and

three Pilates sessions over a week period. During the first two sessions of Pilates, the

emphasis is on activating the deep abdominal muscles associated to the breathing

technique. To be eligible the volunteers could not be engaged in regular exercise

programs during the previous year and had to be classified as ‘minimally active’ or

‘inactive’ using the short version of the International Physical Activity Questionnaire

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(27), so muscle adaptations were not biased due to training, masking the effect of

breathing and/or drawing-in maneuver on lower limb’s muscle recruitment. In addition,

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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 deep tendon reflexes compromise (9).
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Another assessment by a trained Pilates instructor verified the ability to perform

the drawing-in maneuver by using manual palpation at the TrA/IO site (5). All subjects

were able to sustain the TrA/IO recruitment for at least 15 seconds.

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Procedures
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All data was 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

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and it was controlled by the therapist using a chronometer (VOLLO™ VL-501 Digital

Chronometer, 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-min 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

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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

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during the squats to increase the abdominal pressure by pulling the abdominal walls to

the inside by contracting the transverse abdominal and oblique abdominal muscles (29).

During the drawing-in maneuver with Pilates breathing condition (III), the subjects
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were instructed to use the Pilates breathing technique associated to 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
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training were given to ensure that the pelvis was kept leveled and the trunk and the head
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were maintained in vertical alignment.

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Data collection equipment and analysis

A surface electromyographer with eight 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 RMS and impedance of

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109 ohms. The sEMG signals were recorded with surface MEDITRACE™ Ag/AgCl

electrodes with a centre to centre 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 SENIAM recommendations

(http://seniam.org/sensor_location.htm). A reference electrode was placed on the left

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lateral humeral epicondyle. Prior to fixation, the skin was cleaned with 70% alcohol

followed by exfoliation using a sand paper for skin and a second cleaning with alcohol.

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The signals were synchronized using the MIOTEC SUITE™ software with a

sagittal plane video recorded using a webcam (LOGITECH™ C615, Hong Kong,

China). The sEMG signals were amplified and filtered (Butterworth fourth order; 20-
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450 Hz bandpass filter), and the root mean square (RMS) of the data was windowed at

125 ms. All sEMG data were normalized to the three highest peaks, and the mean

muscle activity was calculated from 2-second windows for each squat phase. A blinded

rater experienced with video motion analysis identified the squat phases at specific
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video frames on each participant’s recording using the MIOTEC SUITE™. The rater
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determined the knee flexion peaks, classifying the frames before and after that as the

flexion and extension phasesStatistical analyses

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The Shapiro-Wilk test was used to test the Gaussian distribution of the data.

Normality was accepted, and a 2-way ANOVA was used to assess differences between

phases and among conditions (with LSD t test as a post hoc), and interactions between

conditions (I, II and III) and phases (flexion, extension). The significance was set at

p≤0.05. All statistical analyses were done using the PASW 18.0 statistical software

(SPSS Inc.).

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RESULTS

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

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sEMG means and standard deviations during the flexion phase. Significant differences

among the three conditions were noted during the flexion phase for the rectus femoris,

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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
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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

to condition I.

TABLE 1 HERE
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Table 2 shows the normalized sEMG means and standard deviations during the
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extension phase. Significant differences among the three conditions were noted during

the extension phase for the gastrocnemius medialis, with increased activity during
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condition I compared to II and III.

TABLE 2 HERE

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

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all conditions (p<0.003), and the medial gastrocnemius activity was higher during the

extension phase in condition I (p=0.01).

DISCUSSION

Squats performed with abdominal drawing-in and Pilates breathing resulted in

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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

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60-degree 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
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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 co-contraction to promote

stability for limbs’ movements (4,42). Pilates breathing uses similar stabilization
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techniques during exercises by encouraging co-contraction of core muscles, and the

results (increased stabilization) seems to be similar for the lower limb muscles during
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squats. It has been suggested that reduced anterior tibial translation is associated with

increased hamstrings activation (15), and the ability to increase hamstrings recruitment
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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 (co-contraction) 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 and

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colleagues (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 co-contracting with the gastrocnemius (35), an increased

muscle recruitment in conditions II and III compared I is likely to have occurred to

increase joint stabilization via increased neural drive (3,13).

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Similarly to our findings, a study of deep loaded squats found low level of

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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
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flexion phase, but during the extension phase the drawing-in maneuver, associated or

not to the breathing technique (conditions II and III), resulted in decreased medial

gastrocnemius activation compared to condition I. Our interpretation is that the medial

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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
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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
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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 have been found during voluntary

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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 to normal breathing (40). Therefore, it is possible

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that purposeful breathing drove the muscle recruitment patterns observed. The Pilates

breathing requires deep breathing while keeping the abdomen pulled in by means of

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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.

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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
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abdominal exercises using the Pilates breathing technique compared to regular breathing
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(5).

A study compared the thickness of the transverse abdominal and internal oblique
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muscles based on ultrasound imaging, and the sEMG activity of the external oblique

muscle in thirty three healthy male while performing the drawing-in maneuver or a

maximum exhalation. Maximum exhalation produced significant increased thickness

and sEMG amplitude compared to 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 the present study, the exception

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was the medial gastrocnemius, which showed decreased level of muscle activation

during the combined technique compared to 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

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squat. Other muscles that exert function on the hip and knee need to be assessed to

support these ideas.

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Some limitations may be addressed in the current 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
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young healthy population. The squats were performed without external load and to sixty

degrees 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
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during the entire experiment’s range of time due to the weather characteristics of the
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city. Also, strength assessments were not obtained in the present study, which could

provide better rationale for the results in a long term exercise program.
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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.

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PRACTICAL APPLICATIONS

The result of the present study suggests an implement for lower limb muscle

activation during a 60 degrees 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

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breathing technique and the drawing-in maneuver when performing the squat only by

adding these two techniques during the squat. This information may assist coach and

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physical therapists in design 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

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load.

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Table 1. Normalized mean and standard deviation of lower limb surface electromyography

TE
during the squat knee flexion phase: during I. normal squat (Normal); II. squat with

drawing-in maneuver (DIM); III. squat with drawing-in maneuver and Pilates breathing

(DIM+B).
EP
Rectus Femoris Biceps Femoris Tibialis Anterior Medial Gastrocnemius

Normal (I) 40 (8) 45 (11) 38 (9) 36 (15)

DIM (II) 43 (7) 45 (10) 48 (8) 39 (13)

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DIM+B (III) 52 (5) 54 (5) 53 (6) 39 (14)

ANOVA F, p 8.2, 0.001 3.6, 0.038 11.1,<0.001 0.2, ns

C

post hoc I vs II - - 0.006 -

A

post hoc I vs III 0.001 0.028 0.001 -

post hoc II vs III 0.008 0.025 - -

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Table 2. Normalized mean and standard deviation of lower limb surface electromyography

D
during the squat knee extension phase: during I. normal squat (Normal); II. squat with drawing-

in maneuver (DIM); III. squat with drawing-in maneuver and Pilates breathing (DIM+B).

TE
Rectus Femoris Biceps Femoris Tibialis Anterior Medial Gastrocnemius

Normal (I) 52 (10) 57 (10) 25 (10) 47 (7)

DIM (II) 56 (9) 57 (9) 30 (10) 40 (7)

EP
DIM+B (III) 55 (8) 57 (8) 28 (9) 38 (10)

ANOVA F,p 0.9, ns 0.01, ns 0.2, ns 4.2, 0.023

- - - 0.035
C

post hoc I vs II

post hoc I vs III - - - 0.009

C

post hoc II vs III - - - -

A

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