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Clinical Biomechanics 29 (2014) 885–891

Contents lists available at ScienceDirect

Clinical Biomechanics
journal homepage: www.elsevier.com/locate/clinbiomech

The variable roles of the upper and lower subscapularis during


shoulder motion
James Wickham c, Tania Pizzari a,b,⁎, Simon Balster d, Charlotte Ganderton b, Lyn Watson b,d
a
Lower Extremity & Gait Studies Research Group, Australia
b
Department of Physiotherapy, La Trobe University, Victoria, Australia
c
School of Biomedical Science, Charles Sturt University, NSW, Australia
d
LifeCare Prahran Sports Medicine, Victoria, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Background: The varied roles of the subscapularis muscle as an internal rotator of the humerus, a shoulder abduc-
Received 13 March 2014 tor, a humeral head depressor and an anterior stabiliser may be a result of differing innervation and lines of
Accepted 29 July 2014 torque between its superior and inferior components. The aims of the study were to investigate the differences
in the level of muscle activation between the upper and lower subscapularis during abduction, flexion, internal
Keywords:
and external rotation movements, and temporal characteristics during abduction and flexion.
Electromyography
Methods: Intramuscular electrodes recorded electromyographic muscle activity from the upper and lower
Shoulder
Subscapularis
subscapularis muscles of the dominant throwing arm of twenty-four normal subjects. Participants completed
Rotator cuff ten repetitions of four shoulder movements — abduction, flexion, internal rotation and external rotation. Muscle
Activation activity was expressed as a percentage of maximum voluntary isometric contraction.
Findings: The lower subscapularis was found to activate at a higher level than the subscapularis during abduction,
flexion and external rotation movements and this was significant during concentric and eccentric phases of
abduction and flexion (b0.001). During internal rotation, upper subscapularis muscle activity mirrored that of
lower subscapularis, with a mean difference of 1.14%. Neither upper nor lower subscapularis had onset data com-
mencing prior to the abduction movement; however upper subscapularis activated significantly later than lower
subscapularis (P = 0.018).
Interpretation: The lower subscapularis has significantly higher muscle activity during shoulder elevation and this
might reflect its greater role as a humeral head depressor and anterior stabiliser.
© 2014 Elsevier Ltd. All rights reserved.

1. Introduction branches (Yung et al., 1996). However, the innervation pattern and or-
igins of the upper and lower subscapular nerves are distinctly variable
The subscapularis muscle is crucial for normal shoulder movement between individuals (Kerr, 1918, Lee et al., 2000, Yung et al., 1996).
as it, along with supraspinatus, infraspinatus and teres minor, provides These variations may indicate differential muscle activity between the
a source of dynamic stability to the glenohumeral joint. Subscapularis is upper and lower subscapularis muscles (Kerr, 1918, McCann et al.,
described as an internal rotator of the humerus (Morag et al., 2011), a 1994). In addition, the broad origins, (Liu et al., 1997) and thus the
shoulder abductor (Liu et al., 1997), a humeral head depressor (Inman differing line of torque of each subscapularis muscle component, may
et al., 1944) and an anterior stabiliser (Ovesen and Nielsen, 1985) that contribute to the inferior and superior portions of this muscle having
counterbalances infraspinatus in the axial plane and provides a power- different actions — accounting for the large number of roles described
ful dynamic buttress on the anterior aspect of the joint (DePalma et al., in previous studies (Inman et al., 1944, Liu et al., 1997, Morag et al.,
1967). 2011, Ovesen and Nielsen, 1985). As such, for a comprehensive under-
The subscapularis muscle is considered to comprise upper and lower standing of the role of the rotator cuff, the differences in the upper
segments that are innervated by two or more separate terminal and lower subscapularis muscle activities during common shoulder
movements are important.
Numerous electromyographic studies have evaluated subscapularis
muscle activity in a normal population during common shoulder move-
⁎ Corresponding author at: Department of Physiotherapy, La Trobe University,
Bundoora, Victoria 3086, Australia. ments (O'Connell et al., 2006, Pearl et al., 1992), rotator cuff rehabilita-
E-mail address: t.pizzari@latrobe.edu.au (T. Pizzari). tion exercises (Ganderton and Pizzari, 2013) and sporting activities

http://dx.doi.org/10.1016/j.clinbiomech.2014.07.003
0268-0033/© 2014 Elsevier Ltd. All rights reserved.
886 J. Wickham et al. / Clinical Biomechanics 29 (2014) 885–891

(DiGiovine et al., 1992, Kadaba et al., 1992, Malanga et al., 1996).


Traditionally, studies have evaluated the subscapularis muscle as a sin-
gle muscle unit (Ganderton and Pizzari, 2013, Malanga et al., 1996).
Decker et al. (2003) differentiated superior and inferior components
in their methodology and found greater activity in the upper
subscapularis muscle compared to the lower subscapularis during the
forward punch, internal rotation at mid and high levels of abduction
and push up plus exercises. Nemeth et al. (1990) found no differences
in electromyographic (EMG) pattern or amplitude, however this was
determined subjectively via visual inspection using raw EMG signal
with no statistical comparison. Two further EMG studies found that
upper and lower portions of subscapularis exhibit differential activity de-
pending on shoulder position. During an internal rotation movement,
upper subscapularis muscle activity remains constant or decreases, and
lower subscapularis increases, with increased range of abduction (from
0 to 90°) (Kadaba et al., 1992, McCann et al., 1994). However both studies
did not statistically analyse the differences between the upper and lower Fig. 1. Ultrasound probe placement for upper and lower subscapularis intramuscular
subscapularis. None of the papers measured the subscapularis activity electrode insertions.
during external rotation. Thus, the primary aim of this study was to inves-
tigate the differences in the upper and lower subscapularis muscle activ-
ities during shoulder abduction, flexion, internal rotation and external
rotation movements and during seven maximum voluntary isometric (abduction, flexion, internal and external rotation) were then
contractions (MVICs). The secondary aim was to evaluate the differences performed. Participants were given a 30 second rest between each rep-
in temporal characteristics (onset and termination) between the upper etition to reduce fatigue effects and the order of these exercises was
and lower subscapularis during abduction and flexion. randomised between participants to prevent order effects. During ab-
duction and flexion movements, participants held a light dumbbell in
2. Method the hand — the weight calculated as 25% of the force output (Lafayette
Manual Muscle Tester positioned on the subjects' wrist) for a maximum
2.1. Participants voluntary isometric contraction (MVIC) performed at 90° abduction
(Wickham et al., 2010).
Twenty-four normal subjects (13 male, 11 female) aged between 18 Participants stood in an anatomical position and performed an ab-
and 37 years (X = 23.6 ± 5.3) volunteered to participate in this re- duction/adduction movement in the coronal plane (for abduction trials)
search study. Normal participants had no past history of shoulder and a flexion movement in the sagittal plane (for flexion trials) within a
pain, injury or surgery, or any allergy to adhesives, and were a sample 10 second recording period. The duration of each repetition was
of convenience from a University population. The La Trobe University standardised by having the investigator count the timing of the move-
Ethics Committee approved all research procedures reported in this ment aloud guided by the timing on the Delsys EMG system. To ensure
study and all participants gave written consent prior to participation. a standardised movement plane, each participant was required to pass
the hand between two chains hanging from the ceiling 20 cm apart
2.2. Material and apparatus (Fig 2).
During rotation trials, participants completed isokinetic external and
Two bipolar fine wire intramuscular electrodes were prepared using internal rotation movements in sitting, with their arm held in 90° of
methods first described by Basmajian and Stecko (1962). Following shoulder abduction in the coronal plane and 90° elbow flexion. For ex-
sterilisation, electrodes were inserted under real time ultrasound (HDI ternal rotation trials, participants moved against the KinCom isokinetic
3000, Universal Diagnostic Solutions, California) guidance into the dynamometer at a velocity of 90° per second from neutral rotation to
upper and lower subscapularis of the dominant throwing arm of the full external rotation, and from a fully externally rotated position to a
participant using a 23-gauge hypodermic needle. The electrode position neutral rotation position for internal rotation trials. This method has
was modified from that described by Nemeth et al. (1990), to allow two been shown to be safe and reliable to measure glenohumeral internal
electrodes to be inserted into the muscle. With the subject lying halfway and external rotation strength (Plotnikoff and MacIntyre, 2002).
between supine and side-lying and with the arm abducted and the hand In addition to the four shoulder movements, based on earlier data
placed behind the head, the lateral border of the scapula was palpated (Wickham et al., 2010), 7 isometric MVICs were performed to allow
with markings for needle insertion placed 20 mm anterior to the lateral the EMG data to be normalized and to allow a comparison between
border at distances of 45–60 mm and 95–110 mm above the inferior upper and lower subscapularis activity. These included: abduction at
angle of the scapula (Fig. 1). Needle insertions varied within these two 90° of shoulder joint elevation in the coronal plane; flexion at 90° of
length ranges due to differences in scapula length and the lack of a shoulder joint elevation in the sagittal plane; internal rotation at 90°
reliable superior landmark in the axilla for standardisation (Wickham of shoulder joint elevation with neutral rotation; external rotation at
et al., 2010). 90° of shoulder joint elevation with neutral rotation; horizontal flexion
An accelerometer angle processor was placed on the participants' at 90° of shoulder joint elevation in coronal plane; retraction done
wrist to measure the start and finish of motion and the shoulder angle seated with arms at sides with subject told to squeeze shoulder blades
during dynamic movements. A Delsys Bagnoli-16 EMG system and its together as hard as possible and extension at 0° of shoulder joint eleva-
associated software analysis package (Delsys Inc., Boston, USA) were tion in the sagittal plane. The decision to include 7 MVIC positions was
used to accurately collect and analyse raw EMG data. made on the recommendation that multiple tests be performed in
order to obtain the optimum maximum value for a muscle's MVIC for
2.3. Procedure subsequent amplitude normalisation (Vera-Garcia et al., 2010). Each
MVIC was held for 5 s and a total of three MVICs were performed for
Participants were permitted to practice the four shoulder move- each movement with a three-minute rest between tests to prevent
ments prior to testing. Ten repetitions of each shoulder movement fatigue limiting maximal output.
J. Wickham et al. / Clinical Biomechanics 29 (2014) 885–891 887

Fig. 2. Dynamic flexion trial. a) Participant ready to commence trial. b) Participants' hand passing through the two chains hanging from the ceiling at 180° flexion.

2.4. Data analysis highly reliable (intraclass correlation coefficient, ICC = 0.98)
(Wickham et al., 2010). Muscle onset was calculated as muscle onset
The data analysis procedures used have been previously described minus the movement onset to determine a value in seconds of when
(Semciw et al., 2012). In brief, EMG data from the upper and lower (before or after) the beginning of the movement onset. Similarly, the
subscapularis muscles during abduction, flexion, internal and external termination was determined by taking the value (degrees) when the
rotation movements and the seven maximum voluntary isometric amplitude first dropped below the same amplitude threshold level on
contractions were full wave rectified and low pass filtered at a cut-off the Y axis at which the onset was found (Wickham et al., 2010). Tempo-
frequency of 6 Hz through a 4th order Butterworth filter with phase ral data for the rotation motions could not be obtained due to the use of
lag. To obtain graphs for the isotonic movements, data was time normal- the isokinetic dynamometer.
ised to 100 points (Chapman et al., 2006, Franettovich et al., 2010). Where data were normally distributed, a paired t-test was
Repetitions 4, 5, 6 and 7 were used to calculate RMS values in order to performed to compare %MVIC, onset and termination between the
reduce learning and fatigue effects (Malanga et al., 1996, Myers et al., upper and lower subscapularis and where data violated assumptions
2005, Yasojima et al., 2008). of normality, a Wilcoxon signed-rank test was performed using IBM
To obtain the highest MVIC reference value, all MVIC positions were SPSS (Version 19). To prevent committing a type II error in this explor-
analysed for each muscle. The MVIC value was derived from the highest atory study, a Bonferroni adjustment was not performed and an alpha of
average intensity (root mean square: RMS) from a 600 ms window N0.05 was used (Perneger, 1998). To provide an estimate of the magni-
taken from the middle of the recorded MVIC traces. The highest ampli- tude of difference (effect size, ES) between the upper and lower
tude value across the seven maximum voluntary isometric contractions subscapularis, a standardised mean difference (SMD = mean differ-
was considered the MVIC for each segment for each participant and ence/pooled SD) was calculated for all t-test comparisons. Where
used to formulate the box-plots in Fig. 4. The RMS values obtained Wilcoxon signed-rank tests were performed, a standardised effect size
from muscle onset to termination during the movement trials were was calculated by dividing the z-score of the Wilcoxon signed-rank
expressed as a percentage of the MVIC (%MVIC) value for each muscle. test by the square root of the total sample size (Field, 2013).
Muscle onset and termination data were calculated for the abduc-
tion and flexion motions using the methods described by Wickham 3. Results
et al. (2010), where muscle onset was visually determined as the first
detectable rise from the fluctuating baseline and to avoid bias the re- Mean (standard deviation: SD) muscle intensity, or median (inter-
searcher was blinded to the goniometer trace (Wickham and Brown, quartile range: IQR) muscle intensity and overall average contraction
2012). This visual method of onset determination has been shown to intensity (RMS) values for the upper and lower subscapularis muscles
be highly repeatable and correlated with computer derived methods were compared during four shoulder movements in a normal popula-
(Hodges and Bui, 1996). This exact onset method has been used previ- tion (Table 1). Fig. 3a and b illustrates grand ensembles of the upper
ously by the authors of the current study and has been shown to be and lower subscapularis muscle activities during abduction and flexion
888 J. Wickham et al. / Clinical Biomechanics 29 (2014) 885–891

Table 1
%MVIC mean (standard deviation), median (inter-quartile range) and P-value for upper and lower subscapularis muscles during abduction, flexion, and internal and external rotation.

Movement Phase Muscle Mean (SD) Median (IQR) P-value Effect size

Abduction Concentric Upper subscapularis 6.99(3.79) 6.65(6.85) b0.001a 1.43


Lower subscapularis 13.60(6.26) 15.53(11.97)
Eccentric Upper subscapularis 5.05(1.79) 5.53(2.71) b0.001a 1.41
Lower subscapularis 9.95(4.24) 11.39(5.46)
Total Upper subscapularis 8.68(8.09) 5.67(10.66) 0.018a 0.56
Lower subscapularis 16.25(14.57) 12.53(14.78)
a
Flexion Concentric Upper subscapularis 1.72(0.55) 1.99(0.88) b0.001 1.45
Lower subscapularis 9.17(3.49) 10.87(5.91)
Eccentric Upper subscapularis 1.93(0.36) 1.87(0.52) b0.001a 1.46
Lower subscapularis 6.01(2.57) 6.12(4.86)
Total Upper subscapularis 2.26(2.88) 1.49(1.58) 0.071a 0.43
Lower subscapularis 10.23(14.57) 3.43(12.59)
a
External rotation Total Upper subscapularis 3.73(3.38) 2.24(3.23) 0.831 0.03
Lower subscapularis 9.10(16.97) 2.30(7.47)
b
Internal rotation Total Upper subscapularis 44.46(17.19) 45.64(26.01) 0.836 1.04
Lower subscapularis 43.32(18.31) 42.89(23.65)

Bold indicates significant P-value.


SD = Standard deviation.
IQR = Inter-quartile range.
a
Derived from a Wilcoxon signed-rank test.
b
Derived from a paired t-test.

respectively. The time to peak (accelerometer) is shown as a solid line movement duration. During abduction, two peaks in the upper and
on both ensembles. During abduction, the peak movement occurred at lower subscapularis muscle activities occurred throughout mid-range
4.10 s and at 51% of the movement duration, whereas during flexion, abduction and adduction (at approximately 30% and 70% of the duration
time to peak of the accelerometer was earlier, 3.96 s and 49.5% of the of the movement). During flexion, although not significant (P = 0.07)
differences in the upper and lower subscapularis activities are apparent,
however, the upper subscapularis was below the accepted minimum
detectable level (b 10% MVIC) throughout the entirety of the movement
(Brown et al., 2007).
Overall, the lower subscapularis activated at a higher level than the
upper subscapularis during abduction, flexion and external rotation
movements (Table 1). However, significant differences were identified
only during abduction (P = 0.018, ES = 0.56), with a trend towards sig-
nificance in the flexion movement (Fig. 3b). During internal rotation,
the high %MVIC in upper subscapularis mirrored that of lower
subscapularis, with a mean difference of only 1.14%.
Further analysing the concentric and eccentric phases of abduction,
differences in the upper and lower subscapularis activities were identi-
fied (P b 0.001) with effect sizes of 1.43 and 1.41 respectively. Similarly,
significant differences were seen in the concentric (P b 0.001; ES =
1.45), and eccentric phases (P b 0.001; ES = 1.46) of flexion.
Temporal characteristics (onset and termination) between the two
segments for abduction were compared (Table 2). Temporal data during
the flexion motion were not compared due to the minimal detectable
activity of subscapularis. Muscle onset data revealed that neither
upper nor lower segments were active prior to the abduction move-
ment commencing, as indicated by positive values. However upper
subscapularis activated significantly later than lower subscapularis
(P = 0.018). There was no difference in the point in the movement
where termination of muscle activity occurred.
Extension, internal rotation and horizontal flexion MVICs produced
the greatest muscle activity in the upper and lower subscapularis.
Box-plots illustrating the amplitude of muscle activity between upper
subscapularis (US) and lower subscapularis (LS) during these MVIC ac-
tions are shown in Fig. 4. No statistically significant differences were
found between the two portions of subscapularis.

4. Discussion

This study has shown that there is significantly greater muscle activ-
ity in the lower subscapularis in comparison to the upper subscapularis
during abduction and flexion in a normal population. Additionally,
Fig. 3. Grand ensemble curves for upper and lower subscapularis during abduction (a) and lower subscapularis activated significantly earlier than the upper
flexion (b). segment in abduction. This may indicate different roles for each
J. Wickham et al. / Clinical Biomechanics 29 (2014) 885–891 889

Table 2
Onset and termination during dynamic shoulder abduction in seconds.

Temporal measure Upper subscapularis Lower subscapularis P-value Effect size


Mean (SD) Mean (SD)

Onset (seconds) 0.558(0.33) 0.290(0.16) 0.018a 1.40


Termination (degrees) 16.3(9.4) 19.0(12.2) 0.593b 1.63

SD = Standard deviation.
a
Derived from a Wilcoxon signed-rank test.
b
Derived from a paired t-test.

segment during some shoulder motions and a different functional role subscapularis acts in a similar manner to supraspinatus during eleva-
in the initiation of movement. tion, whereby a large moment arm allows for greater torque production
The increased lower subscapularis activity during elevation might be with a smaller amount of force.
attributed to its greater role in resisting the superior shear force of the Overall the lower subscapularis appears to play a substantial role in
deltoid. The line of pull of the inferior segment of the subscapularis is the normal functioning of shoulder elevation and this has implications
considered to facilitate greater humeral head depression when com- for clinical practice. The inferior portion of the muscle is considered to
pared with the upper segment (Halder et al., 2000). During flexion in be mechanically weak (Halder et al., 2000), and more susceptible to in-
the current study, upper subscapularis was found to be minimally active jury (Piasecki and Nicholson, 2008), and injury to this segment results
according to the classification system used in Yamaguchi et al. (1997). in greater functional limitations (Collin et al., 2013).
This is supported by the results of Collin et al. (2013) who found partic- Both segments of the subscapularis were markedly active
ipants with a muscle tear in their supraspinatus and their upper (Yamaguchi et al., 1997) during the extension MVIC. This supports the
subscapularis, had near full range of movement into forward flexion role of the subscapularis in providing a dynamic buttress on the anterior
(177.5°), however, those who had a tear in supraspinatus and both aspect of the joint to counterbalance powerful posterior muscle activity
their upper and lower subscapularis, had a reduced forward flexion of (DePalma et al., 1967). The markedly active results during internal
83.0°. The significant loss of range identified by Collin et al. (2013) rotation and moderate to moderately strong activity during horizontal
and the increase in lower subscapularis muscle activity in the current flexion MVICs support the belief that subscapularis is a prime mover
study might be attributed to its role in preserving forward flexion by during these movements.
maintaining humeral head centralisation. Onset and termination data showed lower subscapularis to activate
In addition to the lower subscapularis role of humeral head depres- significantly earlier than upper subscapularis during abduction. The ear-
sor, when the arm is positioned in the middle ranges of abduction the lier activation may reflect the lower segments' greater role in humeral
inferior portion of the subscapularis is positioned anterosuperiorly and head centralisation. It could be hypothesised that the muscle activates
contributes the majority of resistance to anterior translation (Halder earlier in readiness to counteract the shear force of the deltoid. A
et al., 2000). This could also explain the greater muscle activity number of studies have examined the temporal characteristics of
identified in the lower segment in the middle of the concentric and ec- subscapularis during various movements and activities (Decker et al.,
centric abduction phases and the large effect sizes between the muscles. 2003, Mulroy et al., 1996), however, only one differentiated timing
The two distinct bursts of activity are likely to be due to the anterior and between the upper and lower subscapularis (O'Connell et al., 2006).
posterior rotators working in a co-ordinated manner to maintain Contrary to the results of this study, O'Connell et al. (2006) found
dynamic stability of the glenohumeral joint through the middle range upper subscapularis to activate significantly earlier than lower
of the movement (Halder et al., 2000, Reinold et al., 2007). subscapularis with a mean latency of 1.26 s between the portions.
Cadaveric modelling has also identified that the superior portion of Whether these differences were found solely during flexion, abduction
the subscapularis muscle is thicker, has a larger abduction moment or both movements combined was not indicated. Additionally, differ-
arm, and can generate greater abduction torque than the inferior ences in results may be due to small sample size (six) and limited num-
portion (Klapper et al., 1992, Otis et al., 1994). Whereas, the lower ber of repetitions (three) analysed in the study by O'Connell et al.
subscapularis produces a large amount of muscle force with a smaller (2006).
moment arm to enhance the dynamic stability of the joint (DePalma Furthermore, O'Connell et al. (2006) reported greater muscle activi-
et al., 1967, Otis et al., 1994). Thus, it could be theorised that upper ty in upper subscapularis in five out of six participants during abduction,

Fig. 4. Box-plots illustrating differences between upper subscapularis (US) and lower subscapularis (LS) during MVIC actions. Box-plots represent median (solid line), inter-quartile range
(edge of the box), and range (upper and lower whisker). ES, effect size.
890 J. Wickham et al. / Clinical Biomechanics 29 (2014) 885–891

scaption, and flexion in the sagittal planes. However, differences were population and likely reflects its greater role as a humeral head depres-
not statistically compared and cannot be assumed to be significantly sor and anterior stabiliser. No differences were found between superior
different. In fact, one of the six participants had the opposite result, and inferior components of subscapularis during internal and external
where higher activity was seen in the lower portion of subscapularis rotation. These differences have potential implications for the interpre-
during elevation — indicating that the natural variability could have a tation of studies of subscapularis activity and function and for the devel-
substantial influence on results with a small sample. In comparison to opment and prescription of rehabilitation exercises. The role of the
the current study, electrode insertions were based on a protocol by different segments needs further analysis since there is limited agree-
Kadaba et al. (1992) and participants completed only three repetitions ment between studies to date.
of each movement at an unknown speed of motion with no resistance.
The findings of the current study add to the confusing picture of the Conflict of interest statement
differing roles of the muscle segments in internal rotation. No difference
was found between the upper and lower segments during an isokinetic None of the authors of the above manuscript has declared any
internal rotation movement at 90° of abduction in this study and during conflict of interest that may arise from being named as an author on
an isometric contraction in the same position. In comparison, Decker the manuscript. There are no known conflicts of interest.
et al. (2003) found the greatest upper subscapularis muscle activity dur-
ing internal rotation at 90° of abduction, while Kadaba et al. found the
opposite, with upper subscapularis decreasing significantly in activity Acknowledgements
throughout the abduction movement from 0 to 90° and generally
performing at a smaller amplitude than lower subscapularis. The No funding was received for the completion of this study.
varying rotation motions may have produced the differing results —
participants in the study by Kadaba et al. (1992) completed one isomet- References
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