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Quadriceps effort during squat exercise
depends on hip extensor muscle
strategy
Megan A. Bryantona, Jason P. Careyb, Michael D. Kennedyc & Loren
Z.F. Chiua
a Neuromusculoskeletal Mechanics Research Program, Faculty
of Physical Education and Recreation, University of Alberta,
Edmonton, Canada
b Department of Mechanical Engineering, University of Alberta,
Edmonton, Canada
c Faculty of Physical Education and Recreation, University of
Alberta, Edmonton, Canada
Published online: 21 Apr 2015.
To cite this article: Megan A. Bryanton, Jason P. Carey, Michael D. Kennedy & Loren Z.F. Chiu
(2015): Quadriceps effort during squat exercise depends on hip extensor muscle strategy, Sports
Biomechanics, DOI: 10.1080/14763141.2015.1024716
To link to this article: http://dx.doi.org/10.1080/14763141.2015.1024716
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Quadriceps effort during squat exercise depends on
hip extensor muscle strategy
MEGAN A. BRYANTON
1
, JASON P. CAREY
2
, MICHAEL D. KENNEDY
3
,&
LOREN Z.F. CHIU
1
1
Neuromusculoskeletal Mechanics Research Program, Faculty of Physical Education and Recreation,
University of Alberta, Edmonton, Canada,
2
Department of Mechanical Engineering, University of
Alberta, Edmonton, Canada, and
3
Faculty of Physical Education and Recreation, University of Alberta,
Edmonton, Canada
(Received 5 April 2013;accepted 19 February 2015)
Abstract
Hip extensor strategy, specifically relative contribution of gluteus maximus versus hamstrings, will
influence quadriceps effort required during squat exercise, as hamstrings and quadriceps co-contract at
the knee. This research examined the effects of hip extensor strategy on quadriceps relative muscular
effort (RME) during barbell squat. Inverse dynamics-based torque-driven musculoskeletal models
were developed to account for hamstrings co-contraction. Net joint moments were calculated using 3D
motion analysis and force platform data. Hamstrings co-contraction was modelled under two
assumptions: (1) equivalent gluteus maximus and hamstrings activation (Model 1) and (2) preferential
gluteus maximus activation (Model 2). Quadriceps RME, the ratio of quadriceps moment to maximum
knee extensor strength, was determined using inverse dynamics only, Model 1 and Model 2.
Quadriceps RME was greater in both Models 1 and 2 than inverse dynamics only at barbell loads of
50–90% one repetition maximum. The highest quadriceps RMEs were 120 ^36% and 87 ^28% in
Models 1 and 2, respectively, which suggests that barbell squats are only feasible using the Model 2
strategy prioritising gluteus maximus versus hamstrings activation. These results indicate that
developing strength in both gluteus maximus and quadriceps is essential for lifting heavy loads in squat
exercise.
Keywords: Knee, hamstrings, gluteus maximus, co-contraction, musculoskeletal modelling
Introduction
Muscle strength has been identified as an important physical fitness quality required for
sports performance. One muscle group where a high level of strength is required across a
range of tasks is the quadriceps. Early research identified positive associations between
quadriceps muscle fibre properties and performance in running and jumping (Bosco &
Komi, 1979). More recently, computer modelling studies have found strengthening of the
knee extensors to have a greater effect on improving vertical jump height than strengthening
of the hip extensors and ankle plantar-flexors (Cheng, 2008; Nagano & Gerritsen, 2001).
q2015 Taylor & Francis
Correspondence: Loren Z.F. Chiu, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, Canada,
E-mail: loren.chiu@ualberta.ca
Sports Biomechanics, 2015
http://dx.doi.org/10.1080/14763141.2015.1024716
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Similar to the propulsion phase of jumping, the knee extensors play a dominant role when
landing from a jump (Moolyk, Carey, & Chiu, 2013). Individuals who have insufficient
quadriceps strength require a change in their movement mechanics, commonly referred to as
compensatory strategies, to perform tasks (Li & Zhang, 1999; Puniello, McGibbon, &
Krebs, 2001; Salem, Salinas, & Harding, 2003). These compensatory strategies, however,
have negative consequences, such as reduction in dynamic stability and increased joint
loading (Puniello et al., 2001).
In order to improve quadriceps strength, exercise selection is critical. Although single-joint
exercises such as weighted leg extensions would appear to strengthen the quadriceps, their
transfer to performance of multi-joint tasks such as jumping is limited (Augustsson, Esko,
Thomee
´, & Svantesson, 1998). Multi-joint exercises such as barbell squats and leg press
have been advocated to improve strength and performance (Augustsson et al., 1998;
Escamilla et al., 2001). However, there is discrepancy in the literature as to the ability for
strength adaptations from these exercises to transfer to performance. Recently, Hartmann
et al. (2012) reported that squat depth was an important variable associated with the
effectiveness of squat exercise. Squats performed to 608knee flexion did not improve
quadriceps strength and vertical jump performance, whereas deep squats did. This finding
may be explained by research which describes knee extensor relative muscular effort (RME)
to be highest in squats performed to knee flexion angles of 105 –1198versus lesser knee
flexion angles (Bryanton, Kennedy, Carey, & Chiu, 2012).
RME is the ratio of the moment required for an activity relative to the moment generated
during a maximal voluntary contraction (MVC). Although knee extensor RME was highest
in a deep squat, this value was only 57% MVC utilising a barbell load of 90% one repetition
maximum (1 RM) (Bryanton et al., 2012). Exercises for muscle strengthening are most
effective when muscles are generating greater than 80% MVC, as recruitment of high
threshold motor units is achieved at this contraction force level (Fry, 2004; Peterson, Rhea,
& Alvar, 2004). This suggests that knee extensor RME achieved during deep squat exercise
should be too low to optimally stimulate strength adaptations. It has been suggested that
squat exercise is a hip extensor dominant task, which is supported by reports of greater
hip than knee extensor net joint moment (NJM) and RME (Bryanton et al., 2012; Flanagan
& Salem, 2008). However, hip extensor RME is still less than 80% MVC, thus squat exercise
may not sufficiently activate high threshold motor units to optimise strength development of
the hip extensor musculature. The low knee extensor RME, however, may be explained by a
limitation of the inverse dynamics analysis used in Bryanton et al. (2012). Inverse dynamics
calculates NJM, which is the sum of all moments acting at a joint. While the primary
contributor to the knee extensor NJM is the quadriceps moment, co-contraction of the
hamstrings would generate a flexor moment at the knee (Rao, Amarantini, & Berton, 2009).
Thus, when the hamstrings co-contract, knee extensor NJM is less than quadriceps moment.
Subsequently, knee extensor RME would be less than quadriceps RME.
In Bryanton et al. (2012), hip extensor RME was 76% MVC at 90% 1 RM. The gluteus
maximus and hamstrings each contribute approximately 45–55% of the moment generated
during a hip extensor MVC (Waters, Perry, McDaniels, & House, 1974). Thus, the
hip extensor RME during barbell squats requires both gluteus maximus and hamstrings
activation. As hamstrings activation is required for hip extension for barbell squat exercise, their
co-contraction effect at the knee suggests that quadriceps RME during barbell squats is greater
than the 57% MVC previously reported (Bryanton et al., 2012). Moreover, the hip extensor
strategy, specifically the contribution of gluteus maximus versus hamstrings to hip extension,
will influence the amount of hamstrings co-contraction and subsequently quadriceps RME.
Three assumptions for hip extensor strategies are possible: (1) equivalent activation, (2)
2M.A. Bryanton et al.
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monoarticular dominant, and (3) biarticular dominant. The equivalent activation strategy has
equal gluteus maximus and hamstrings activation. The monoarticular dominant strategy
requires the gluteus maximus to be activated maximally before the hamstrings activate
(Basmajian & Latif, 1957; Travill, 1962). The biarticular dominant strategy is the reverse
where the hamstrings activate maximally before gluteus maximus activation.
As different hip extensor strategies are possible, and the biarticular hip extensors
(i.e. hamstrings) co-contract with the quadriceps at the knee, the hip extensor strategy
employed will influence the quadriceps RME. However, the gluteus maximus and
hamstrings are often considered to be synergists due to their shared hip extension action and
the term ‘posterior chain’ has arisen from the exercise literature to describe these muscles as
a functional grouping (De Ridder, Van Oosterwijck, Vleeming, Vanderstraeten, & Danneels,
2013; Frost, Abdoli-e, & Stevenson, 2009). This is in contrast to the anatomical,
biomechanical, and clinical literature describing the differences between gluteus maximus
versus hamstrings (Jacobs, Bobbert, & van Ingen Schenau, 1996; Wagner et al., 2010;
Waters et al., 1974). As a consequence, it is important to understand whether the
hip extensor muscles operate as independent muscles or as a single functional group.
As the amount of hamstrings co-contraction present will influence the quadriceps force
required to extend the knee, the purpose of the current investigation was to evaluate how
hip extensor strategy influences quadriceps RME during squat exercise. The data used for
analysis were from our previous investigation (Bryanton et al., 2012). An inverse dynamics-
based torque-driven musculoskeletal model was developed to estimate quadriceps NJM
using knee extensor NJM and accounting for the hamstrings moment at the knee. The
amount of hamstrings co-contraction modelled was dependent on the assumptions
underlying the three hip extensor strategies. From initial calculations, a biarticular dominant
strategy was considered impossible, as the estimated quadriceps RME exceeded 100% MVC
even at low barbell loads (50% 1 RM). Therefore, two models were developed, one for the
equivalent activation (Model 1) and one for the monoarticular (Model 2) strategy. It was
hypothesised that (1) accounting for hamstrings co-contraction using Models 1 and 2 would
result in quadriceps RME greater than inverse dynamics calculated knee extensor RME; and
(2) Model 1 would provide the upper and Model 2 the lower bounds for quadriceps RME
during barbell squat exercise.
Methods
Participants
Ten women with minimum one year experience performing the back squat and capable
of squatting a minimum barbell load equal to their body mass were recruited. Participants
were 22.5 ^2.1 years of age, were 1.68 ^0.09 m tall, had 62.5 ^6.5 kg body mass, and had
a 1 RM back squat of 80.5 ^10.1 kg. All participants currently used squat exercise in their
training regimens and no participants reported musculoskeletal injuries. Study procedures
were explained to participants who provided written informed consent as approved by the
Physical Education and Recreation and Agricultural, Life and Environmental Research
Ethics Board at the University of Alberta (study ID: Pro00016957).
Data collection
Data collection is described in detail in Bryanton et al. (2012). Participants completed three
sessions: (1) back squat 1 RM testing; (2) motion analysis of squats performed at 50%, 60%,
Hip extensor strategy and quadriceps effort during squat exercise 3
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70%, 80%, and 90% 1 RM; and (3) maximum muscle strength testing, spaced approximately
one week apart. Motion analysis was performed using nine optoelectronic Pro-Reflex
MCU240 cameras (Qualisys AB, Gothenburg, Sweden) and kinetic data captured from two
OR6-6 force platforms (AMTI, Watertown, MA, USA) sampling at 120 Hz and 1200 Hz,
respectively. Reflective markers were placed on the lower extremity and reconstructed using
Visual 3D (version 4.82; C-Motion, Germantown, MD, USA) to compute hip, knee, and
ankle angles and NJM.
Muscle strength testing involved single-joint maximal voluntary isometric contractions
using a custom-built dynamometer. Knee extensor testing was performed seated with the
participant’s hip at approximately 908. Hip extensor testing was performed supine. Isometric
testing was considered justified as pilot research found joint angular velocities during the
concentric phase of squatting were between 308/s and 608/s; and it is equivocal whether
maximum voluntary torque measurements are different between these joint angular
velocities during isokinetic testing versus isometric testing, particularly when matched for
joint angle and controlling for the isovelocity period (Perrine & Edgerton, 1978; Prietto &
Caiozzo, 1989). Participants performed maximum hip extensor, knee extensor, and ankle
plantar-flexor actions at multiple joint angles. Force was measured using an MLP-350 load
cell (Transducer Techniques, Temecula, CA, USA) channelled through a TMO-1-2200
signal conditioner (Transducer Techniques), digitally converted using a 12-bit PCI-DAS
120/JR analog-to-digital board (Measurement Computing, Norton, MA, USA) and
sampled at 500 Hz using APAS software (Ariel Dynamics, Temecula, CA, USA). Moment
was calculated by multiplying force by the moment arm of the dynamometer pulley.
Moments were corrected for the effect of limb segment weights by manually measuring limb
lengths and angles at each position; and calculating their inertial effect using Dempster’s
anthropometric parameters (Winter, 2009). For each muscle group, the relation between
moment and joint angle were fit with regression equations to generate a strength curve. RME
was calculated by taking the ratio of NJM to the moment from the strength curve at the same
joint angle and expressed as a percentage (i.e. % MVC).
Co-contraction modelling
Modelling was performed using Microsoft Excel 2007 (Microsoft Corporation, Redmond,
WA, USA). The first step in modelling was determining load sharing between the hamstrings
and gluteus maximus. Waters et al. (1974) determined maximum total hip extensor
moment, and then using sciatic nerve block, hip extensor moment from the gluteus maximus
alone. Contribution of the hamstrings was therefore total hip extensor moment minus
gluteus maximus moment. Data from Waters et al. (1974) for 158,458, and 908hip flexion
were fit with a second-order polynomial:
%HS½h¼20:00456h2þ0:50436hþ34:97063 ð1Þ
%GM½h¼0:00456h220:50436hþ65:02937 ð2Þ
where %HS[h] and %GM[h] are percentage contribution of hamstrings and gluteus
maximus, respectively, to maximum hip extensor moment for a given hip angle (h).
Two sub-models were developed with different assumptions. In Model 1, it was assumed
hamstrings and gluteus maximus were equally activated regardless of hip extensor RME.
That is, hamstrings and gluteus maximus were active at the same percentage of their
4M.A. Bryanton et al.
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maximum moment-generating ability. For Model 1, hamstring moment at the hip was
estimated by multiplying hip extensor NJM with percentage contribution of hamstrings at
the corresponding hip joint angle:
MHH1½h¼%HS½h£NJMHip½hð3Þ
where M
HH1
[h] is hamstrings moment at the hip for Model 1 and NJM
Hip
[h] is the
hip extensor NJM calculated from motion analysis data.
In Model 2, it was assumed the hamstrings did not activate until gluteus maximus reached
its maximum moment generating ability. For example, if hip extensor RME was 70% MVC
and gluteus maximus contributed 52% of the maximum hip extensor moment, hamstrings
contribution would be 18% (70%-52% ¼18%). Hamstrings moment for Model 2
(M
HH2
[h]) was calculated as
MHH2½h¼NJMHip ½h2%GM½h£MVCHE½hð4Þ
where MVC
HE
[h] is the measured maximum strength of the hip extensors. Model 2 was
based on research demonstrating a hierarchical order for activating synergist muscles
(Basmajian & Latif, 1957; Travill, 1962; Zhang & Nuber, 2000), where monoarticular
muscles (i.e. gluteus maximus) are activated prior to biarticular muscles (i.e. hamstrings).
It is likely that neither model is perfectly valid; however, Model 1 would represent an upper
limit and Model 2 the minimum hamstrings co-contraction; defining upper and lower bound
values for the true quadriceps moment.
Hamstrings moment arm at the hip was determined from Ne
´meth and Ohlse
´n(1985) who
reported the moment arm of the hamstrings acting at the hip joint at 58intervals from 08to
908of hip flexion. A second-order polynomial regression was fit to these data to allow greater
precision in determining hamstrings moment arm at the hip:
rHH½h¼20:01003h2þ0:69911hþ57:90441 ð5Þ
where r
HH
[h] is hamstrings moment arm at the hip. Hamstrings muscle force was estimated
by dividing hamstrings moment at the hip by hamstrings moment arm at the hip for the
corresponding joint angle:
FH½h¼MHH½h
rHH½hð6Þ
where F
H
[h] is hamstrings force.
Wretenberg, Nemeth, Lamontagne, and Lundin (1996) used identical methods to
Ne
´meth and Ohlse
´n(1985) to determine moment arms of biceps femoris—long head,
semitendinosus, and semimembranosus acting at the knee. These data were best fit using
second-order polynomials:
rBF½k¼20:0034k2þ0:2633kþ16:80 ð7Þ
rST½k¼0:0022k2þ0:0133kþ27:30 ð8Þ
rSM½k¼0:0032k220:0433kþ20:60 ð9Þ
Hip extensor strategy and quadriceps effort during squat exercise 5
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where r
BF
[k], r
ST
[k], and r
BF
[k] are moment arms at the knee of biceps femoris—long head,
semitendinosus, and semimembranosus, respectively, at a given knee angle (k). As each of
the three hamstrings muscles have unique distal attachments, each muscle had a different
knee flexor moment arm. Physiological cross-sectional areas of individual hamstrings
muscles were taken from Woodley & Mercer (2005) to determine load sharing among the
hamstrings. The total hamstrings physiological cross-sectional area was determined and
physiological cross-sectional area of each individual muscle was expressed as a percentage of
the total. This assumes that all hamstrings muscles have the same specific tension. Force in
each hamstrings muscle was their percentage total physiological cross-sectional area
multiplied by estimated total hamstrings force. Moment generated by each hamstrings was
calculated as cross-product of moment arm and force for semitendinosus, semimembra-
nosus, and biceps femoris—long head individually, and then summed giving hamstrings
moment at the knee:
MHK½k¼rBF ½k£ð0:2968 £FH½hÞþrST½k£ð0:2384 £FH½hÞþrSM ½k£ð0:4647 £FH½hÞ ð10Þ
where M
HK
[k] is hamstrings moment at the knee.
Quadriceps moment was estimated as the sum of knee extensor NJM and hamstrings
moment at the knee:
MQ½k¼NJMKnee½kþMHK ½kð11Þ
where M
Q
[k] is quadriceps moment. Quadriceps RME was determined as the ratio of
quadriceps moment to maximum isometric quadriceps moment at the corresponding joint
angle and expressed as a percentage:
RMEQ½k¼MQ½k
MO
Q½k
£100% ð12Þ
where MO
Q½kis maximum isometric quadriceps moment.
Squat depth was operationally defined as knee joint angle, where 08is full extension, and
increasing angle refers to knee flexion. Quadriceps RME was determined at 158intervals
from 308to 1198knee flexion (30 – 448,45–598,60–748,75–898, 90 – 1048, and 105– 1198)
using software code written in Matlab (Mathworks, Natick, MA, USA). Data from 0 – 298
knee angles were not analysed as knee and hip flexor moments were present during these
squat depths and were not of interest for this investigation.
Statistical analysis
For statistical analyses, RME data were averaged across limbs as well as between repetitions
at the same barbell load. Assumption of data normality was confirmed using Q– Q plots
(Wilk & Gnanadesikan, 1968). To examine the research hypothesis that quadriceps RME
would be different between the three methods of estimation (knee extensor NJM, Model 1
and Model 2), 3 (method) £6 (squat depth) repeated measures ANOVA was used to
examine RME. Separate ANOVA were conducted for each barbell load. Where significant,
Tukey HSD was used for subsequent post hoc comparisons of method and squat depth.
Alpha was set a priori at
a
¼0.05. ANOVA were performed in SPSS (version 11.0; SPSS
Inc., Chicago, IL, USA). Q – Q plots and Tukey HSD were performed using Microsoft Excel
2007. Data are presented as mean ^standard deviation.
6M.A. Bryanton et al.
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Results
Representative figures for quadriceps RME estimated using Models 1 and 2 are presented in
Figure 1. The highest RME estimated were 120 ^36% MVC in Model 1 and 87 ^28%
MVC in Model 2. Significant model by squat depth interactions were found for all barbell
loads ( p,0.001). Average quadriceps RME estimated using each method are displayed in
Figures 2 (50% 1RM), 3 (60% 1 RM), 4 (70% 1 RM), 5 (80% 1 RM), and 6 (90% 1 RM).
At 50% and 60% 1 RM loads, quadriceps RME was greater in Model 2 than both Model 1
and knee extensor NJM at all squat depths except 30 – 448(p#0.05). At 70%, 80%, and
90% 1 RM, quadriceps RME was greater in Model 2 than both Model 1 and knee extensor
NJM at all squat depths ( p,0.05). Quadriceps RME was greater in Model 1 versus knee
extensor NJM at 60% 1 RM for the 105 –1198depth; at 60% 1 RM for 90 – 1048and 105–
1198; at 80% 1 RM for all depths except 30–448; and at 90% 1 RM for all depths ( p,0.05).
For clarity, statistical differences for squat depth are only reported between successive
squat depths (e.g. between 30– 448and 45 – 598or between 45– 598and 60 –748). For the
knee extensor method, quadriceps RME was greater at 45 – 598than 30– 448for all barbell
loads and at 105 – 1198than 90 –1048for 70%, 80%, and 90% 1 RM loads ( p,0.05).
For Model 1, quadriceps RME was greater at 45 – 598than 30– 448and at 105 –1198than
90–1048for all barbell loads ( p,0.05). At 80% 1 RM, quadriceps RME was also greater at
60–748than 45 – 598using Model 1 ( p,0.05). For Model 2, quadriceps RME was greater
Figure 1. Plots of knee extensor (solid line), Model 1 quadriceps (dashed line), and Model 2 quadriceps (dotted line)
relative muscular effort versus squat depth (knee flexion angle) for a representative participant with a barbell load of
90% 1 RM.
Hip extensor strategy and quadriceps effort during squat exercise 7
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at 45– 598versus 30 – 448,60–748versus 45– 598, 90 – 1048versus 75 – 898, and 105 –1198
versus 90– 1048for all barbell loads ( p,0.05).
Discussion and implications
The purpose of this research was to examine how hip extensor strategy (equal activation
versus monoarticular dominant) would influence quadriceps RME during squat exercise.
The primary finding of this research is that accounting for hamstrings co-contraction results
in quadriceps RME higher than previously reported knee extensor RME (Bryanton et al.,
2012). As the actual hip extensor strategy used during squat exercise is not known, it was
hypothesised that the two models used would provide upper (Model 1) and lower (Model 2)
bounds for quadriceps RME. However, Model 1 does not appear to be feasible for barbell
squat exercise. At 50% 1 RM, quadriceps RME modelled using Model 1 is 100% MVC and
increases for heavier barbell loads. These high quadriceps RME occur at knee flexion angles
of 105– 1198, which means that an individual squatting to this depth using the equivalent
activation strategy would not be able to rise out of the squat (see Figures 3 – 6). Therefore,
the only viable hip extensor strategy for performing barbell squat exercise to knee flexion
angles greater than 1058is the monoarticular strategy. The monoarticular strategy has
previously been described for single-joint tasks such as elbow flexion and extension
(Basmajian & Latif, 1957; Travill, 1962). The rationale for this strategy is that biarticular
Figure 2. Quadriceps relative muscular effort from knee extensor net joint moment (circles), Model 1 (squares), and
Model 2 (diamonds) at 50% 1 RM. *Indicates significant difference from knee extensor net joint moment
(p,0.05); #indicates significant difference from Model 2 ( p,0.05);
a
indicates significant difference from
preceding squat depth ( p,0.05).
8M.A. Bryanton et al.
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muscles generate an undesired action at adjacent joints which must be neutralised by other
muscles. In the case of squat exercise, the undesired action by the biarticular hamstrings is a
knee flexor moment which is antagonistic to the extensor moment required at the knee.
The average quadriceps RME at 90% 1 RM was 87 ^28% MVC using Model 2. As such,
quadriceps strength is one limiting factor in the ability to lift heavy barbell loads in squat
exercise. However, Model 2 assumes that gluteus maximus activation is maximal; therefore
gluteus maximus RME must be 100% MVC. Accordingly, gluteus maximus strength is also
a limiting factor in squat performance. Therefore, the current findings indicate that the
quadriceps and gluteus maximus operate synergistically during squat exercise. Increasing the
contribution of the gluteus maximus to hip extensor NJM reduces hamstrings co-contraction
at the knee. Consequently, it can be suggested that maximising gluteus maximus and
minimising hamstrings activation is required for lifting the heaviest weight possible in squat
exercise. EMG is typically used to compare activation between muscles; however, there are
few reports investigating both gluteus maximus and hamstrings during squat exercise. EMG
data presented by Robertson, Wilson, and St. Pierre (2008) indicate lower inter-subject
variability for gluteus maximus versus biceps femoris and semimembranosus, particularly at
the initiation of the concentric phase where quadriceps RME is greatest. The low variability
observed for gluteus maximus indicates that this muscle is uniformly active across
individuals. However, greater variability for the hamstrings suggests a range of activation
levels across individuals. This would support the present findings that gluteus maximus is the
Figure 3. Quadriceps relative muscular effort from knee extensor net joint moment (circles), Model 1 (squares), and
Model 2 (diamonds) at 60% 1 RM. *indicates significant difference from knee extensor net joint moment
(p,0.05); #indicates significant difference from Model 2 ( p,0.05);
a
indicates significant difference from
preceding squat depth ( p,0.05).
Hip extensor strategy and quadriceps effort during squat exercise 9
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primary hip extensor in squat exercise and that hamstrings contribution varies depending on
the remaining hip extensor NJM required.
Previous research on squat mechanics, as well as coaching literature, has suggested that
either a hip extensor or knee extensor dominant technique may be employed for squat
exercise (Flanagan & Salem, 2008; Fry, Smith, & Schilling, 2003). The knee extensor
dominant technique, which is associated with a high bar placement, requires greater ankle
dorsiflexion with the torso in a vertical position. The hip extensor dominant technique,
associated with a low bar placement, requires less ankle dorsiflexion but greater forward
torso rotation (Fry et al., 2003). This distinction of hip versus knee strategies has also been
used to describe vertical jumping (Vanrenterghem, Lees, & De Clercq, 2008). However, a
simple division of effort between muscles at the hip versus muscles at the knee is not
justifiable. In tasks where hip extensor RME exceeds approximately 50% MVC, a shift to a
so-called hip extensor dominant strategy requires greater hamstrings activation. Although
this strategy appears to shift mechanical effort from the knee to the hip, knee extension is still
required, thus quadriceps activation would have to remain high to counteract the flexor effect
of the hamstrings at the knee. As such, hamstrings co-contraction masks the true quadriceps
effort when using inverse dynamics analysis. This has previously been recognised by
Doorenbosch, Harlaar, Roebroeck, & Lankhorst (1994), who observed a substantial
decrease in knee extensor NJM but minimal change in quadriceps EMG when shifting from
knee to hip strategies during the sit-to-stand task.
Figure 4. Quadriceps relative muscular effort from knee extensor net joint moment (circles), Model 1 (squares), and
Model 2 (diamonds) at 70% 1 RM. *Indicates significant difference from knee extensor net joint moment
(p,0.05); #indicates significant difference from Model 2 ( p,0.05);
a
indicates significant difference from
preceding squat depth ( p,0.05).
10 M.A. Bryanton et al.
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For this reason, in multi-joint tasks requiring hip and knee extensor NJM, the so-called
hip extensor versus knee extensor dominant classification is not valid. Rather, squat-type
tasks should be classified by where they lie along the continuum of monoarticular versus
biarticular dominant hip extensor strategies. The monoarticular dominant strategy would
minimise hamstrings activation and subsequent co-contraction at the knee. This strategy
would appear to be most appropriate for tasks requiring a high knee extensor NJM. High
knee extensor NJM are present in tasks with large vertical ground reaction forces and large
leg dorsiflexion angles (Chizewski & Chiu, 2012; Moolyk et al., 2013). These mechanics
commonly occur in sport, particularly when landing from a jump (Moolyk et al., 2013).
As such, a monoarticular dominant hip extensor strategy may be required for jump landings
and the ability to use such a strategy is dependent on the strength of the gluteus maximus.
Therefore, preferential resistance training of gluteus maximus and not the hamstrings
muscles would be warranted.
However, specific functions of biarticular muscles have been identified, which suggest that
biarticular dominant strategies may be preferred in some tasks. The hamstrings transfer
energy between the hip and knee joints in running, jumping, cycling, and skating, as well as
alter the direction of the ground reaction force during forward and backward jumping
(Jacobs et al., 1996; Jacobs & van Ingen Schenau, 1992; Mathiyakom, McNitt-Gray, &
Wilcox, 2007; van Ingen Schenau, 1989). Due to the antagonistic actions of the hamstrings
and quadriceps, a task using the biarticular dominant strategy requires one or both of the
Figure 5. Quadriceps relative muscular effort from knee extensor net joint moment (circles), Model 1 (squares), and
Model 2 (diamonds) at 80% 1 RM. *Indicates significant difference from knee extensor net joint moment
(p,0.05); #indicates significant difference from Model 2 ( p,0.05);
a
indicates significant difference from
preceding squat depth ( p,0.05).
Hip extensor strategy and quadriceps effort during squat exercise 11
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following conditions to be met. The first condition is if hip extension occurs prior to knee
extension. A temporal delay between hip and knee extensions could create a time lag
between peak hamstrings and quadriceps moments at the knee (Ravn et al., 1999).
Therefore, it is possible for both the hamstrings and quadriceps to generate large flexor and
extensor moments, respectively, at the knee, provided they do not occur simultaneously.
Earlier extension of the hip than the knee is a feature of multi-joint tasks such as vertical
jumping (van Ingen Schenau, 1989).
The second condition is sufficiently strong quadriceps. Stronger quadriceps are able to
tolerate greater hamstrings co-contraction. It has been suggested that hamstrings activation
reduces anterior tibial translation which is associated with anterior cruciate ligament injury
(Ford, Myer, Schmitt, Uhl, & Hewett, 2011). Recent investigations have found that when
the height of landing increases, quadriceps but not hamstrings EMG activity increases (Ford
et al., 2011; Peng, Kernozek, & Song, 2011). These results are interpreted as a
neuromuscular deficit in utilising the hamstrings, which is suggested to predispose an
individual to anterior cruciate ligament injury. However, considering the results of the
current investigation, it could also be hypothesised that the ability to increase hamstrings
activation is limited by quadriceps strength. To land from a jump, a minimum knee extensor
NJM is required, which increases with greater landing height. As the knee extensor NJM is
composed of agonist (i.e. quadriceps) and antagonist (i.e. hamstrings) moments, an
increased hamstrings moment would require an increased quadriceps moment to generate
Figure 6. Quadriceps relative muscular effort from knee extensor net joint moment (circles), Model 1 (squares), and
Model 2 (diamonds) at 90% 1 RM. *Indicates significant difference from knee extensor net joint moment
(p,0.05); #indicates significant difference from Model 2 ( p,0.05);
a
indicates significant difference from
preceding squat depth ( p,0.05).
12 M.A. Bryanton et al.
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the same knee extensor NJM. If individuals have weak quadriceps, greater hamstrings
activation is not possible, as it would shift the knee extensor NJM towards a knee flexor NJM,
preventing the task from being performed. Therefore, athletes performing tasks, such as
landing from a jump, that have high knee extensor NJM should increase the strength of their
quadriceps.
The relations between the gluteus maximus, hamstrings, and quadriceps are also relevant
to consider for other knee injuries. If the gluteus maximus is weak relative to the hamstrings,
the contribution of the hamstrings to the hip extensor NJM required for a task increases.
A recent case study hypothesised this to be the cause of hamstrings overexertion resulting in
exercise-induced hamstrings cramping (Wagner et al., 2010). A rehabilitation programme
strengthening the gluteus maximus resolved the exercise-induced hamstrings cramping.
Although a case study alone does not provide conclusive evidence, in conjunction with the
present study, it supports the hypothesis that gluteus maximus weakness may result in
hamstrings overexertion and subsequently injury. Quadriceps force generates patellofemoral
joint pressure (Powers, Chen, Scher, & Lee, 2006; Powers, Lilley, & Lee, 1998). Hamstrings
co-contraction increases quadriceps force and patellofemoral pressure to magnitudes that
may cause patellofemoral pain syndrome (Elias et al., 2011). Either or both deficient gluteus
maximus strength and incorrect technique requiring excessive hip extensor NJM may be
implicated in exaggerated hamstrings co-contraction at the knee. By altering technique to
involve less hip extensor NJM, hamstrings, and concomitantly quadriceps, activation would
decrease, reducing patellofemoral pressure. As such, a comparison of gluteus maximus
versus hamstrings would be important to examine whether a monoarticular or biarticular
hip extensor strategy is employed. This may be performed, experimentally and clinically,
using EMG.
As with any musculoskeletal modelling approach, the findings of the current paper are
subject to assumptions and limitations. One limitation is that Models 1 and 2 accounted for
the biarticular hamstrings muscles which cross the hip and knee. The rectus femoris, a
quadriceps muscle, also crosses both joints; however, the hip flexor effect of the rectus
femoris was not included in the models. The hip flexor action of rectus femoris should have
only a small effect on the results. From Bryanton et al. (2012) and the current paper, the
highest hip extensor, knee extensor, and quadriceps RME occur at the 105 –1198knee
flexion angle squat depth when using a high bar technique. The moment arm for rectus
femoris at the hip decreases with increasing hip flexion compared to the moment arm for the
hamstrings at the knee which either remains constant or increases with greater knee flexion
(Visser, Hoogkamer, Bobbert, & Huijing, 1990; Wretenberg et al., 1996). As the hip flexor
action of rectus femoris and the knee flexor action of the hamstrings are antagonistic to the
hip and knee extensor NJM, this suggests that the effect of the hamstrings at the knee is
greater than the effect of rectus femoris at the hip at greater squat depths. Furthermore, the
rectus femoris contributes approximately 20% of the total quadriceps moment during
maximum isometric knee extensor actions at 608knee flexion (Zhang, Wang, Nuber, Press,
& Koh, 2003) and is estimated to contribute 23% of total quadriceps force based on
physiological cross-sectional area measurements (Narici, Landoni, & Minetti, 1992).
In contrast, the hamstrings contribute approximately 50% of the total hip extensor moment
during maximum isometric actions (Waters et al., 1974). Taken together, the relatively low
force generated by the rectus femoris and its small moment arm for hip flexion at high
hip flexion angles suggest that the hip flexor moment from rectus femoris would be small.
Moreover, a hip flexor moment generated by the rectus femoris would require greater
hip extensor moments from either gluteus maximus or hamstrings. This would further
support the importance of training the monoarticular muscles—gluteus maximus and the
Hip extensor strategy and quadriceps effort during squat exercise 13
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vasti—to perform activities with high hip and knee extensor NJM. Therefore, this limitation
may have a small influence on the exact quantitative results; however, it would not change the
interpretation of the results.
In this study, it is assumed that the strength measurements represent the maximum force
generating ability of the muscles at a given joint angle. To accomplish this, a curve fitting
technique was used to extrapolate data for angles not tested. Curve fitting may influence the
data at a specific joint angle. To reduce the effect of errors with curve fitting influencing a
specific joint angle, data were averaged across bins of 158knee flexion range of motion. This
method of ‘binning’ data is common in EMG investigations of exercises to represent muscle
electrical activity across portions of the range of motion (Ninos, Irrgang, Burdett, & Weiss,
1997). It may also be argued that because of biarticular muscles, hip angle will influence
knee extensor strength and, similarly, knee angle will influence hip extensor strength
(Deighan, Serpell, Bitcon, & De Ste Croix, 2012; Waters et al., 1974). However, Waters
et al. (1974), found knee flexion angle had little effect on maximum hip extensor strength.
Similarly, Deighan et al. (2012) found no difference between knee extensor strength in
seated versus supine positions for isokinetic testing at slow speeds. Nonetheless, for this
investigation, knee extensor strength testing was performed seated and the knee was flexed in
hip extensor strength testing, which approximate the combinations of hip and knee angles
when quadriceps RME was greatest. Finally, contributions of the individual quadriceps
components may vary, particularly for open- versus closed-kinetic chain activities. In open-
kinetic chain activities such as isometric knee extension testing, all four quadriceps muscles
are active (Salzman, Torburn, & Perry, 1993), whereas in closed-kinetic chain tasks, such as
cycling and rowing, contribution of the vasti are greater than that of the rectus femoris (Chin
et al., 2011; Endo et al., 2007; Gue
´vel et al., 2011). Thus, if rectus femoris is not fully active
in squat exercise, knee extensor strength testing may generate greater MVC torque than
would be possible during squat exercise. Therefore, quadriceps RME would be higher than
calculated, providing greater support for the use of a gluteus maximus hip extensor strategy.
In summary, this research modelled hamstrings co-contraction to improve estimates of
quadriceps RME during barbell squat exercise. In barbell squats, hamstrings activation must
be minimised so that its co-contraction at the knee does not require the quadriceps moment
to exceed its strength capacity; therefore, a hip extensor strategy prioritising the gluteus
maximus is required. Both gluteus maximus and quadriceps are limiting factors in the ability
to squat heavy barbell loads. This contradicts previous descriptions of hip extensor versus
knee extensor dominant strategies, a classification schema that does not appear to be valid.
Rather, multi-joint tasks requiring hip and knee extensor efforts should be classified based on
their hip extensor strategy—either monoarticular or biarticular dominant—as the relative
contribution of gluteus maximus versus hamstrings will influence quadriceps RME. Full
squat exercise is limited by the strength of both the quadriceps and gluteus maximus;
therefore, to improve squat performance, these muscles should be targeted in resistance
training. The synergy between and strength development for these muscles should also be
considered in other tasks where high quadriceps efforts are required, such as jump landing
(Moolyk et al., 2013). The present study confirms Bryanton et al.’ (2012) finding that
quadriceps loading is dependent on squat depth and a depth greater than 1058knee flexion is
required to maximally load these muscles. Full squats should be employed to strengthen the
quadriceps and improve performance of tasks requiring quadriceps strength, such as vertical
jumping (Hartmann et al., 2012). Contrary to common perceptions of the hip extensor
musculature (De Ridder et al., 2013), the gluteus maximus and hamstrings may not function
synergistically. Greater hamstrings co-contraction at the knee may increase patellofemoral
contact pressure and patellar ligament tension, which are associated with patellofemoral pain
14 M.A. Bryanton et al.
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syndrome and patellar tendinitis, respectively. Gluteus maximus weakness and incorrect
technique causing excessive hip extensor NJM should be considered factors that may
predispose individuals to these knee injuries.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This research was funded by a Graduate Research Grant from the National Strength and
Conditioning Association Foundation.
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