Revista Brasileira de Fisioterapia 1413-3555: Issn: Rbfisio@
Revista Brasileira de Fisioterapia 1413-3555: Issn: Rbfisio@
Revista Brasileira de Fisioterapia 1413-3555: Issn: Rbfisio@
ISSN: 1413-3555
rbfisio@ufscar.br
Associação Brasileira de Pesquisa e Pós-
Graduação em Fisioterapia
Brasil
Felício, Lilian R.; Dias, Luiza A.; Silva, Ana P. M. C.; Oliveira, Anamaria S.; Bevilaqua-Grossi, Débora
Ativação muscular estabilizadora da patela e do quadril durante exercícios de agachamento em
indivíduos saudáveis
Revista Brasileira de Fisioterapia, vol. 15, núm. 3, mayo-junio, 2011, pp. 206-211
Associação Brasileira de Pesquisa e Pós-Graduação em Fisioterapia
São Carlos, Brasil
Lilian R. Felício1, Luiza A. Dias2, Ana P. M. C. Silva2, Anamaria S. Oliveira3, Débora Bevilaqua-Grossi3
Abstract
Background: Hip and knee muscle weaknesses have been associated with the onset of anterior knee pain (AKP). Therefore, the
understanding of how squats exercises can be performed in order to optimize the electrical activity of these muscles is relevant for
physical therapy treatments. Objective: To compare the electromyographic activity of patella and pelvic stabilizers during traditional
squat and squat associated with isometric hip adduction or abduction in subjects without AKP. Methods: Electromyography signals were
captured using double-differential electrodes at the vastus medialis obliquus (VMO), vastus lateralis obliquus (VLO), vastus lateralis
longus (VLL) and gluteus medium (GMed) in 15 healthy and sedentary women during squats exercises: traditional and associated with
hip adduction and hip abduction with load of 25% of body weight. Linear mixed models with significance level of 5% were used for data
analysis. Results: Squat associated with hip adduction and abduction produced electromyographic activity of GMed of 0.47 (0.2) and
0.59 (0.22) respectively, while conventional squat produced an electromyiographic activity of 0.33 (0.27). The higher VMO activity was
0.59 (0.27) during the isometric contraction in the squat associated with hip adduction. The higher VLO activity was 0.60 (0.32) during
isometric contraction in the squat associated with hip abduction. Conclusion: Squat exercise associated with hip adduction increased
VMO muscle activity as well as the activity of GMed activity.
Resumo
Contextualização: Atualmente relaciona-se a fraqueza dos músculos do quadril e da coxa ao surgimento da dor anterior no joelho
(DAJ). Dessa maneira, compreender como os agachamentos devem ser realizados para melhorar a ativação elétrica desses músculos
é importante para o tratamento fisioterapêutico. Objetivo: Comparar a ativação dos estabilizadores da patela e pelve entre as posições
de agachamento convencional e associado à contração isométrica em adução e abdução da coxa em indivíduos sem queixa de
DAJ. Métodos: O sinal eletromiográfico foi captado a partir de eletrodos duplo-diferenciais posicionados nos músculos vasto medial
oblíquo (VMO), vasto lateral oblíquo (VLO), vasto lateral longo (VLL) e glúteo médio (GMed) em 15 mulheres sedentárias e clinicamente
saudáveis, durante a contração de agachamento convencional e associados à adução e à abdução isométrica da coxa com carga de
25% do peso corporal. A análise estatística empregada foi o modelo linear de efeitos mistos, com significância de 5%. Resultados: A
associação da adução e abdução isométrica da coxa no agachamento produziu cerca de 0,47 (0,2) e 0,59 (0,22), respectivamente,
de atividade elétrica do músculo GMed, enquanto o agachamento convencional (AGA) produziu 0,33 (0,27) de atividade elétrica. A
maior ativação do VMO aconteceu na contração de agachamento associado à adução da coxa e foi de 0,59 (0,27); já o músculo VLL
apresentou uma maior atividade elétrica durante o agachamento associado à abdução, sendo de 0,60 (0,32). Conclusão: O exercício
de agachamento associado à adução da coxa promoveu uma maior ativação muscular do VMO, além de aumentar a atividade
muscular do GMed.
1
Postgraduate Program of Health Science Applied of Locomotor Apparatus, School of Medicine from Ribeirão Preto (FMRP), Universidade de São Paulo (USP), Ribeirão Preto, SP, Brazil
2
Course of Physical Therapy, FMRP, USP
3
Department of Biomechanics, Medicine and Rehabilitation of the Locomotor System, FMRP, USP
Correspondence to: Lilian Ramiro Felício, Av. Bandeirantes, 3900 CEP 14049-900, Ribeirão Preto, SP, Brasil, e-mail: lilianrf@uol.com.br
206
Rev Bras Fisioter. 2011;15(3):206-11.
Muscle activity in squat
Introduction Methods
Squat exercises are often prescribed in physiotherapy Fifteen sedentary women with no AKP complain were
practice for several knee impairments because when prop- recruited through verbal invitation and participated in this
erly administered, it promotes an increase in knee and pel- study. Inclusion criteria were women that presented with a
vic muscles strenght1-3. In addition, this exercise in closed maximum of two clinical signals of misalignment in the lower
kinetic chain is an integral part of functional activities and limb12, with no complains of AKP13, and no history of orthope-
these exercises are often related with pain in patient with dic or neurological conditions, trauma or previous surgery of
anterior knee pain (AKP) such as sport practices and going bones, muscles and joints of the lower limb or spine, since pain
up and down stairs1. is the main complain associated to AKP. Exclusion criteria was
Exercises in closed kinetic chain associated to isometric complain of pain in any part of the lower limb and performance
contractions of hip abductors generate a higher electrical of any type of physical activity, recreational or sportive, twice or
activation of the gluteus medium muscle (GMed) in healthy more frequently per week6.
subjects when compared to the exercises done in opened All of the participants were properly informed about the
kinetic chain. Additionally, the bipodal squat produces a study procedures and signed a free informed consent approved
better pelvic stabilization when compared to the unipodal by the Ethics Research Committee of the Clinical Hospital of
squat4. Furthermore, although the associations of isometric the Medical School of Ribeirão Preto, Ribeirão Preto, SP, Brazil
hip adduction and abduction have been reported to pro- (protocol nº. HCFMRP 14102/2006).
duce an increased activity of GMed during bipodal squats, The surface electromygraphic signals were collected
the same has been found not to be true when considering bilaterally from eight double-differentials active electrodes
unipodal squats. with three Ag/AgCl bars (dimensions 23x21x5 mm and dis-
The squat with the association of isometric contraction tance between electrodes of 10 mm), with gain of 20x, input
of hip adduction has been shown to promote values of elec- impedance of 10GΩ and band-pass filter and the common
tromyographic amplitude similar for the medial and lateral mode rejection ratio of the 130dB. The active electrodes
portions of the quadriceps. Therefore, this squat modality pro- were positioned on the vastus medialis obliquus (VMO),
motes a better balance of the patellofemoral joint in compari- vastus lateralis obliquus (VLO), vastus lateralis longus (VLL)
son to the conventional squat (CS)6. However, these studies6 (Figure 1A)14 and GMed (Figure 1B)15. They were fixed with a
did not evaluate the pelvic musculature. double-sided adhesive tape to the skin previously prepared
Understanding how squats can be performed in order to and the connections were tested according to the rules of
promote a higher activation of patella and hip stabilizers is the Surface EMG for Non Invasive Assessment of Muscles Proj-
relevant because in addition to the dynamic stability of the ect15. The stainless steel ground electrode (diameter of 3 cm)
patella, weaknesses of pelvic stabilizer are related to patel- was fixed to the sternum.
lofemoral dysfunction7-11. The signals were analogically amplified and digitalized
There is no description in the literature regarding the most with simultaneous frequency of sampling of 2 KHz by chan-
efficient way to perform squat exercises in order to promote nel, in the range of 0.01–1.5 kHz, by the convertor board of
balanced activation of the dynamic stabilizers of the patella 16 bits of resolution of dynamic range from the portable
and a higher electrical activity of the pelvic stabilizers. This
information will help provide scientific basis and justification
for the prescription of squat exercise for patients with AKP or
patellofemoral dysfunction.
In this context, the purpose of the present study was to
compare the electromyographyc activity of the patella and
hip stabilizers between the positions of conventional squat
and squats associated with isometric contraction of hip ad-
duction and abduction in subjects with no complaint of AKP.
The hypothesis of the present study is that squat associated
with isometric contractions of hip abduction generates an Figure 1. Sensors position on the vastus medialis obliquus,
increase in the electromyographic activity of the patella vastus lateralis obliquus and vastus lateralis longus according to
stabilizers when compared to the conventional squats and Bevilaqua-Grossi et al.14(1A), and gluteus medium according to
squats with hip adduction. SENIAM project15(1B).
207
Rev Bras Fisioter. 2011;15(3):206-11.
Lilian R. Felício, Luiza A. Dias, Ana P. M. C. Silva, Anamaria S. Oliveira, Débora Bevilaqua-Grossi
device Myosystem BR-1P84, from the brand Datahominis position of the frontal and transversal planes (Figure 2A). The
(Uberlândia, Minas Gerais, Brazil). The Myosystem Program, squat exercises associated to the MIVC of hip adduction (CS-
version 3.5, was used for visualizing and processing the elec- ADD)6 were performed in the same position of the CS a sup-
tromyographic signal. port positioned between the legs, in the height of the medial
The electromygraphic signals of the VMO, VLO and VL femoral epicondyle (Figure 2B). The squat exercises with hip
were collected during three maximal isometric voluntary abduction (CS-ABD) were performed on the same position as
contractions (MIVC) of shank extension, with the knee fixed the CS with addition of MIVC of hip abduction resisted by an
at 90° of flexion (extensor chair), since this position facili- non elastic band, adjustable with Velcro®, positioned leveled
tates a higher electrical activity of the quadriceps muscles1. with lateral femoral epicondyle (Figure 2C). Pelvic movements
The MIVC of the GMed was collected in the manual muscle in transversal and frontal planes were visually controlled by the
testing position16; with the hips in 20º of abduction and 10º evaluators. The squat contractions were recorded in isometric
of extension. Pelvic stabilization and the resistance imputed position to guarantee that the electromygraphic surfaces were
to the distal portion of the leg were applied manually by the not affected by the variations in tension-length and tension-
same evaluator17. The MIVC of these activities were main- velocity relation or even by the number of motor units active in
tained for six seconds, and were later used as reference values the area of caption19.
for normalization of the electromygraphic data obtained in The sequences of the exercises were determined by a simple
the squat exercises studied. draw and were recorded for six seconds of three contractions
All isometric positions of squats were performed with an for each squats condition. All participants were verbally moti-
additional load of 25% of each subject body weight. This ad- vated during the contractions by the same examiner. A mini-
ditional load was determined by trial and error, in a pilot study. mal resting time of two minutes between each contraction was
This load was identified as the minimal capable load to inten- established to minimize the effects of muscle fatigue20.
sify the myoelectric activity, especially of the muscle GMed, The raw electromyographic signals were digitally filtered
to an acceptable level of signal-noise relation using double- in the band of 20 to 500 Hz, and the root square of the mean
differential electrodes9,14. squares (RMS, root mean square) was calculated to represent
The electromygraphic data of the CS was collected with the amplitude of muscle activation.
the participants with their back supported on a ball of 45 cm The mean value of RMS of each muscle was normalized by
diameter, of the brand Carci®, and maintaining it against a the mean value of the RMS obtained in the contractions of ref-
wall, with 60° of knee flexion18, feet apart and hips in neutral erence of the same muscle21. In other words the RMS was nor-
malized by the relation between the mean value of the studied
contractions and the mean value obtained from the recordings
of MIVCs. Thus, the values of amplitude of myoelectric activa-
tion are presented in arbitrary unit (AU). The muscle activity
was characterized as minimal (between 0 and 0.39), moderate
(between 0.40 and 0.74) and strong (between 0.75 and 1)22.
Means and standard-deviations of the RMS normalized
values were used to verify statistically significant differ-
ences between the dominant and non-dominant sides and
between the different squat conditions. Mixed linear model23
is a test of variance and was used in this study as it takes
into account both the source of variations intra- and inter-
subjects. This statistical method is recommended when the
values of the same subject are grouped, and the assumption
of independence between the observations in the group is
not adequate23. The random effect was considered as being
the muscles assessed, VMO, VLO, VLL and GMed, and the
fixed effect was considered as being the exercises, CS, CS-ABD
Figure 2. Traditional Squat with 60° of knee flexion and hip in
and CS- ADD.
neutral position (2A), squat associated with isometric contraction of
The adjustment of the model for a normal distribution was
hip adduction (2B) and quat associated with isometric contraction of
hip abduction (2C). done through the procedure PROC MIXED uinsg SAS® 9.0.
208
Rev Bras Fisioter. 2011;15(3):206-11.
Muscle activity in squat
Table 2. Mean and standard deviations of the normalized electromyographic amplitudes of the muscles: vastus medialis obliquus (VMO), vastus lateralis
obliquus (VLO), vastus lateralis longus (VLL) and gluteus medium (GMed) during traditional squat (SQ), squat associated with isometric contraction of
the hip abduction (SQ-ABD) and squat associated with isometric contraction of the hip adduction (SQ-ADD). Arbitrary Units (A.U.) (n=15).
Dominant Limb SQ SQ-ABD SQ-ADD
GMED 0.33 (0.27) 0.47 (0.20) a 0.59 (0.22) b
VMO 0.32 (0.12) 0.52 (0.24) 0.59 (0.27) c
VLO 0.32 (0.12) 0.38 (0.17) 0.41 (0.11)
a
VLL 0.37 (0.14) 0.60 (0.32) 0.53 (0.16) b
Non-dominat Limb
GMED 0.26 (0.13) 0.52 (0.24) a 0.59 (0.27) b
VMO 0.46 (0.33) 0.38 (0.25) 0.58 (0.59) c
VLO 0.35 (0.14) 0.37 (0.15) 0.44 (0.15)
VLL 0.49 (0.19) 0.53 (0.19) 0.61 (0.28)
a b c
Significant difference between SQ-ABD and SQ p<0.05; Significant difference between SQ-ADD and SQ p<0.05; Significant difference between SQ-ADD and SQ-ABD p<0.05.
209
Rev Bras Fisioter. 2011;15(3):206-11.
Lilian R. Felício, Luiza A. Dias, Ana P. M. C. Silva, Anamaria S. Oliveira, Débora Bevilaqua-Grossi
VMO muscle, which are desirable activations in the rehabilitation the hip abductors muscles. Furthermore, the tensor fasciae
of meniscal27 and ligament28 of the knee and in the AKP29,30. latae muscle is an anterior-lateral stabilizer of the knee, and
Moreover, the results of this study revealed that squat with a weakness in this musculature can lead to increased shear
hip abduction stimulated the activation of the GMed but also forces and hence an increase in patellofemoral stress31.
provided higher activity of the VLL. This greater activation of Finally, it is important to consider that this is an explor-
the VLL should not be advocated in the intervention of patel- atory study and its results, as the variance of the average EMG
lar dislocations and patellofemoral dysfunctions, since it could amplitude, can be used as a basis for further studies that seek
favor the lateralization of the patella1. to replicate this method with a larger number of participants,
Coqueiro et al.6 reported that the prescription of exercises as well as with AKP patients, highlighting the therapeutic value
that promote muscle synergism of the patella lateral stabilizer of these exercises.
musculature are as important as promoting the contraction of
the medial portion of the quadriceps. Our data do not differ
with regards to the activation of GMed and indicate a balanced Conclusion
activity between the stabilizers of the patella in the exercises
CS-ADD and CS-ABD, but the squat exercise associated with The results of this study showed that the squat exercise as-
adduction of the hip showed an increase in the myoelectric sociated with hip adduction produced higher activation of the
activity of the muscle VMO. It is suggested, therefore, that this VMO muscle, and produced an increase in the activity of the
exercise is the most suitable in the rehabilitation of patients GMed.
with AKP, since it emphasizes the GMed activation and the
activity of VMO.
The results of this study are limited by the lack of informa- Acknowledgements
tion about the kinematics of the pelvis and lower limb seg-
ments and the exact change of the patella positioning caused To the Fundação de Amparo à Pesquisa do Estado de São
by the muscle contractions proposed. Another aspect that was Paulo - FAPESP (process number 2007/08461-6), for the finan-
not addressed is the relationship between the muscle tensor cial support, and to the Center of Quantitative Methods- CE-
fasciae latae and its function of pelvic stabilizer together with MEQ/Clinical Hospital, FMRP, for the statistical analysis
References
1. Escamilla RF, Zheng N, Macleod TD, Brent Edwards W, Imamura R, Hreljac A, et al. with patellofemoral pain. Med Sci Sports Exerc. 2007;39(8):1227-32.
Patellofemoral joint force and stress during the wall squat and one-leg squat. Med Sci Sports
11. Bolgla LA, Malone TR, Umberger BR, Uhl TL. Hip strength and hip and knee kinematics during
Exerc. 2009;41(4):879-88.
stair descent in females with and without patellofemoral pain syndrome. J Orthop Sports Phys
2. Dionisio VC, Almeida GL, Duarte M, Hirata RP. Kinematic, kinetic and EMG patterns during Ther. 2008;38(1):12-8.
downward squatting. J Electromyogr Kinesiol. 2008;18(1):134-43.
12. Dye SF. Patellofemoral pain current concepts: an overview. Sports Med Arthrosc. 2001;9(4):
3. Stensdotter AK, Hodges PW, Mellor R, Sundelin G, Häger-Ross C. Quadriceps activation in 264-72.
closed and in open kinetic chain exercise. Med Sci Sports Exerc. 2003;35(12):2043-7.
13. Cowan SM, Bennell KL, Hodges PW, Crossley KM, McConnell J. Simultaneous feedforward
4. Distefano LJ, Blackburn JT, Marshall SW, Padua DA. Gluteal muscle activation during common recruitment of the vasti in untrained postural tasks can be restored by physical therapy. J Orthop
therapeutic exercises. J Orthop Sports Phys Ther. 2009;39(7):532-40. Res. 2003;21(3):553-8.
5. Hertel J, Earl JE, Tsang KK, Miller SJ. Combining isometric knee extension exercises with 14. Bevilaqua-Grossi D, Monteiro-Pedro V, Sousa GC, Silva Z, Bérzin F. Contribution to the
hip adduction or abduction does not increase quadriceps EMG activity. Br J Sports Med. anatomical study of the oblique portion of the vastus lateralis muscle. Braz J Morphol Sci.
2004;38(2):210-3. 2004;21(1):47-52.
6. Coqueiro KRR, Bevilaqua-Grossi D, Bérzin F, Soares AB, Candolo C, Monteiro-Pedro V. Analysis 15. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG
on the activation of the VMO and VLL muscles during semisquat exercises with and without sensors and sensor placement procedures. J Electromyogr Kinesiol. 2000;10(5):361-74.
hip adduction in individualsn with patellofemoral pain syndrome. J Electromyogr Kinesiol.
16. Kendal FP, McCreary EK, Provance PG, Rodgers MM, Roman WA. Muscles: provas e funções. 5ª
2005;15(6):596-603.
Ed. São Paulo: Editora Manole; 2007.
7. Souza RB, Powers CM. Differences in hip kinematics, muscle strength, and muscle
17. Basmajian JV, De Luca CJ. Muscle Alive: their functions revealed by Electromyography. 5ª ed.
activation between subjects with and without patellofemoral pain. J Orthop Sports Phys Ther.
Baltimore: Willians & Wilkins; 1985.
2009;39(1):12-9.
18. Bevilaqua-Grossi D, Felicio LR, Simões R, Coqueiro KRR, Monteiro-Pedro V. Avaliação
8. Ireland ML, Willson JD, Ballantyne BT, Davis IM. Hip strength in females with and without
eletromiográfica dos muscles stabilizers da patella durante exercício isométrico de squat
patellofemoral pain. J Orthop Sports Phys Ther. 2003;33(11):671-6.
em indivíduos com síndrome da dor femoropatellar. Rev Bras Med Esporte. 2005;11(3):
9. Robinson RL, Nee RJ. Analysis of hip strength in females seeking physical therapy treatment for 159-63.
unilateral patellofemoral pain syndrome. J Orthop Sports Phys Ther. 2007;37(5):232-8.
19. De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech.
10. Cichanowski HR, Schmitt JS, Johnson RJ, Niemuth PE. Hip strength in collegiate female athletes 1997;13(2):135-63.
210
Rev Bras Fisioter. 2011;15(3):206-11.
Muscle activity in squat
20. Callaghan MJ, McCarthy CJ, Oldhan JA. Electromyographic fatigue characteristics of the 26. McCrory JL, Quick NE, Shapiro R, Ballantyne BT, McClay Davis I. The effect of a single treatment
quadriceps in patellofemoral pain syndrome. Man Ther. 2001;6(1):27-33. of the Protonics on system biceps femoris and gluteus medius activation during gait and the
lateral step up exercise. Gait Posture. 2004;19(2):148-53.
21. Hanten WP, Schuthies SS. Exercise effect on electromyographic activity of the vastus medialis
oblique and vastus lateralis muscles. Phys Ther. 1990;70(9):561-5. 27. Akima H, Furukawa T. Atrophy of thigh muscles after meniscal lesions and arthroscopic partial
menisectomy. Knee Surg Sports Traumatol Arthrosc. 2005;13(8):632-7.
22. Kelly BT, Backus SI, Warren RF, Williams RJ. Electromyographic analysis and phase definition of
the overhead football throw. Am J Sports Med. 2002;30(6):837-44. 28. Bryant AL, Kelly J, Hohmann E. Neuromuscular adaptations and correlates of knee functionality
following ACL reconstruction. J Orthop Res. 2008;26(1):126-35.
23. Schall R. Estimation in generalized linear models with random effects. Biometrika. 1991;78(4):
719-27. 29. Wilk KE, Reinold MM. Principles of patellofemoral rehabilitation. Sports Med Arthrosc.
2001;9(4):325-36.
24. Nyland J, Kuzemchek S, Parks M, Caborn DN. Femoral anteversion influences vastus medialis
and gluteus medius EMG amplitude: composite hip abductor EMG amplitude ratios during 30. Cabral CMN, Monteiro-Pedro V. Recuperação funcional de indivíduos com disfunção
isometric combined hip abduction-external rotation. J Electromyogr Kinesiol. 2004;14(2): femoropatellar por meio de exercícios em cadeia cinética fechada: revisão da literatura. Rev Bras
255-61. Fisioter. 2003;7(1):1-8.
25. Mascal CL, Landel R, Powers C. Management of patellofemoral pain targeting hip, pelvis, and 31. Cohen M, Vieira EA, Silva RT, Vieira ELC, Berlfein PAS. Estudo anatômico do trato iliotibial:
trunk muscle fuction: 2 case reports. J Orthop Sports Phys Ther. 2003;33(11):647-60. revisão crítica de sua importância na estabilidade do joelho. Rev Bras Ortop. 2002;37(8):
328-35.
211
Rev Bras Fisioter. 2011;15(3):206-11.