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Electromyography of shoulder muscles in relation to force direction
Electromyography of shoulder in relation to force direction Henk J Arwert, MD, MSc, Jurriaan de Groot, Wllbert W and Piet M. Rozing, MD, PhD, leiden, The Ne/her/ands
L M
muscles Van Woensel,
MSc,
In a static force task the electromyographic level of 74 shoulder muscles including 3 rotator cuff muscles was related to force direction. Surface and wire electrodes were used. The force direction of maximal electromyography (principal action) was identified for every muscle. The principal action expresses the function of a muscle in a specific situation. The deltoid was active in a force direction that could be understood from its anatomy. The trapezius and serrafus were main/y involved in stabilizing the scapula in upward and outward force directions. large multiarticular muscles such as the pectoralis and the latissimus were active in downward and forward forces. The rotator cuff seems to have a specific role in stabilizing the gienohumeral joint. These data can be compared with data of patients with shoulder disorders and with kinematic data of a shoulder model. (J SHOULDER E~5ow SURG
1997;6:360-70.1 Ttt e s h ou Id er is an interesting but complex mechanism. It enables us to position the arm and hand effectively in a three-dimensional working space. The shoulder consists of 3 bones, 17 muscles, and 3 joints 28.. the sternoclavicular (SC) joint, the acromioclavicular (AC) joint, and the glenohumeral (GH) joint. All three joints participate in any motion of the shoulder.‘O The underlying causes of some important shoulder disorders such as instability or impingement are still not fully understood. To reveal the cause of these shoulder disorders, more has to be known about the biomechanical and coordinative behavior of the normal shoulder and about the function of shoulder muscles. Recent publications show a growing interest in this subject.5, ‘, 9, 12, 13, la, 25, x The goals of our study included the following. (1) To describe muscle function of the shoulder. In general, electromyography (EMG) can be a useful method to study muscle function, although there
From the State University of leaden, Research Group of Kineslology, Department of Orthopedics, Delft Umvenlty of Technology, Laboratory of Measurement and Control, and AcademIcal Hosprtal of leaden, Department of Orthopedics Reprmt requests Henk J Arwert, MD, MSc, State Unlverslh/ of Leaden. Research Grout of Klnesloioav, Deoortment of Orthopedlcs, Rlinsburgelweg 10, 2333 AA”celden’, The Netherlands CopyrIght Board
0
105%2746/97/$5
360
1997
by Journal
of Shoulder
of Trustees 00 + 0
32/l/79906
ond
Elbow
Surgery
are some technique-related problems.3, 19, 24 (2) To determine to what extent we can derive muscle function from the orientation of a muscle’s lever arm with respect to the joint axis. The EMG results of our study were compared with a biomechanical shoulder model.21, 26, 28 (3) To test our hypothesis that muscle function can depend on shoulder position. We were interested in the relation between the function of shoulder muscles and the position of the shoulder joint. The lever arm of the subscapularis muscle, for example, depends on the position of the GH joint. Because of this, the subscapularis function might be influenced by humeral abduction.16 Special attention was paid to the function of the rotator cuff muscles. As assumed previous4, 6~ 13, 20, 22 indications were found that this IYI muscle group plays a specific role.
METHODS EMG. EMG
of 14 muscles or muscle groups was recorded in two sessions with the use of bipolar surface electrodes or intramuscular wires’, l5 (Table I). The surface electrodes had a fixed interelectrode distance of 21.5 mm. Electrode positions were standardized (Table I). The dual wire electrodes were made of Teflon-coated platinum (0.10 mm). The wires were not insulated at the tip (1 mm); the distance between the tips was 2 mm. The subjects were asked to move their
Atwert
1. Shoulder Elbow 5x-g. Volume 6, Number 4
Table I Muscles
Involved
Muscle
Electrode
DA DM
In this study and the type and posItion Electrode Middle
Surface Surface Surface
DP TD TT
of the muscle
4 cm above
TA
Surface
PMCL PMST
Surface Surface
SA
Surface
6th head
LD IS
Surface Surface
SSP ssc TM DA, Anterior ascending; dorsi, joint,
deltoid; PMCL,
Mlddle
spanned
AC,
the margin
of the muscle.
TS, an % of the line between
of the sternal
TS and
PS.
T8.
SC SC, AC SC, AC AC,
GH GH
6 cm below Al, lateral part Middle of the muscle belly
SC, AC, GH
GH
Wire Wire
Middle Axillar
GH
Surface
3 cm up and
SSP, supraspinatus; Ioint;
KS, scapular
below
part
GH
SC, AC, SC, AC
axillary
fold
of the muscle approach
DM, medial deltoid; DP, posterior pectoralis major, clavicular part,
IS, infrasplnatus, G/i, glenohumeral
Joints
belly
On % of the line between TS and Middle of the clavicular part
lateral
from
GH GH
Al
deltoid; JD, trapezius pectoralis malor,
PMSJ,
SSC, subscapularis; spine; KS, spinal
TM, teres process;
361
of the electrodes
location
Middle of the muscle belly Middle of the muscle belly Right above TS, 2 cm below
Surface Surface
et al.
descending; pars sternal
major; A/, inferior
77, trapezius, transverse; part; SA, serratus anterior,
SC, sternoclavicular angle; MM, medial
joint; AC, margin;
JA, trapezius, ID, latissimus
acromioclavicular J8, eighth thoracic
vertebra.
shoulder as little as possible after insertion of the wires to avoid wrinkling or breakage of the wires. If, however, some scapular motion occurred, the wires slid in and out without wrinkling. Discomfort caused by the wires was minimal once the wires were inserted. At the end of the recording session the wires were removed and checked; no breakage was observed. The EMG signal was preamplified, high-passfiltered (10 Hz), amplified, and stored on tape. Before AD conversion (1000 Hz, 12 bit) an analog low-pass filter (500 Hz) was used. All measurements were performed on the right shoulder. Experimental setup. Five healthy subjects participated in this study (mean age 26 years, 1 man, 4 women). Twelve muscles were recorded in the first session. The subjects were seated in three different positions. Position 1 was 90” scapular abduction, the elbow in a 90” flexed orthosis, and the forearm horizontal. Position 2 was 90” anteflexion of the humerus, the elbow in a 90” flexed orthosis, and the forearm vertical (Figure 1). Position 3 was 90” of anteflexion of the humerus, the elbow in a 90” flexed orthosis, and the forearm horizontal. In the second session we collected the data of two other muscles (teres maior, pectoralis major, sternal portion) in three of the subjects in position 1. A local coordinate system (xyz) was used for the humerus. The y axis was in line with the humeral shaft. The z axis was parallel to the forearm. The x
axis was perpendicular with respect to the y axis and the z axis. A positive moment around the z axis in position 1 and 3 led to a force directed downwards and in position 2 to a medially directed force. A support was provided for the subiect’s head and back. The elbow orthosis was suspended to compensate for gravity. This enabled the subjects to relax their arm in any of the three positions. The elbow orthosis was connected with a strain-gauge two-dimensional force transducer. The two-dimensional force plane was perpendicular to the humerus. This force transducer registrated forces in the x- and z-direction. The subjects were visually informed by means of a monitor about the force vector they exerted (force level and direction). This resultant force vector was digitized and compared with the target force vector that was shown on the monitor. It is important to note that the subjects were not restricted or constrained in humeral axial rotation or backward-forward translations, so the force vector was always perpendicular to the humerus. Because the arm was suspended, no muscle activity was needed to keep the arm in position. Procedure. First, the subjects were asked to relax their shoulder muscles. This was controlled by the EMG. Subsequently the force transducer was set to zero by removing the offset in the x and z directions. Subjects were asked to exert a force in eight alternating directions in the force plane (per-
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SO
Figure and
Table
actual
1 ExperImental force
vector
setup were
II Resultant force directions
Subjects
direction (‘I
0 45
90 135 180 225 270 315 Mean resultant force (N)
able
to see monitor
and force levels averaged Position
Target
were
Resultant direction
On
momtor,
target
force
vector
displayed
(“)
0.9 46.4 90 6 135.3 181.4 224 9 271 3 315 1 140
1
over five sublects, Position
SD
0.8 0.7 0.5 03 0.4 1.3 0.6 1.0 0.2
Resultant direction
0.2 46.5 90.4 135.6 181.3 225.1 270.3 315.4 139
(“)
2
presented
for each Position
SD
0.5 0.8 07 0.5 0.4 12 09 10 03
Resultant direction
0.9 45.4 89.9 135.5 181.2 225.0 269.9 315.5 14.0
(‘)
posltton
3
SD
0.5 0.5 0.6 04 0.4 0.6 0.5 05 07
Target force level was 14 N in every direction.
pendicular to the humerus) without changing their position. The resultant force vector was displayed on the monitor. The task was to aim this vector at one of the displayed targets and to maintain this force for 3 seconds. Eight force directions were studied: 0” (upwards) and clockwise steps of 45”; 90” was directed laterally, 270” medially (Figure 1). The target force level was 14 N in all directions (compensated for gravity). A period of at least 1 second was selected, during which the resultant force vector was constant in magnitude and direc-
tion. The EMG signal was rectified and averaged. One trial consisted of eight alternating force directions; every subject performed three trials in every position. In every trial the highest EMG value of a muscle was set to 100%. The subjects had to practice three trials to become familiar with the force task. Data processing and interpretation. The force direction in which the EMG of a specific muscle was maximal was one of the most important parameters that could be obtained from the EMG
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Table III Descriptive
statistics of the prlnclpal Position
Muscle
Mean 339 21 74 0 56 56 276 260 333 143 34 356 151 149
DA DM DP TD Tr TA PMCL PMST SA LD IS SSP ssc TM Abbreviations
as in Table
action
(In degrees)
1
Position SD 16.3 198 13.6
245 96 14.0 11.0
3.8 66 206 666 28 7 309 10.3
Mean
obtalned
Position
2 Mean
8.0 13.5 18.2 10.2 173 140 9.8 9.2 12.7 28.3 246 31.2
341 127 80 51 171
363
by electromyography
SD
354 20 108 0 70 65 293
et al.
3 SD
333 26 92 9 68 58 290 325 128 68 40 146 -
130 21 2 9.2 25.8 15.3 13.6 10.3 12.0 55 566 307 33.2
I
data. This parameter is called the principal action.17 The principal action was estimated by means of a curve fitting procedure. This was done by applying a second order polynomial fit to the data points that constitute the peak in the EMG/ force direction curves. The principal action is not influenced by normalization methods. We used a kinematic analysis by means of a biomechanical shoulder model that is described in detail by Prank*’ and by Van der Helm et al.26 This three-dimensional model is based on the dissection of cadaver shoulders and consists of 3 joints, 3 ligaments, and 95 muscle elements. This model needs the digitized three-dimensional configuration of the shoulder girdle as input parameters. The procedure to obtain these coordinates is described by Prank.*’ We compared the principal action of each muscle with its mechanical action. The mechanical action was defined as the force vector in the plane of the force transducer that would result from a standardized force of one specific muscle. This standardized force was not related to the crosssectional area or muscle architecture; the mechanical action depends only on the muscle lever arm with respect to a specific joint. This procedure was performed for one of the subjects in position 1, After the bony landmarks of the shoulder were digitized, the model was provided with the necessary parameters to calculate the mechanical action. For every joint these calculations were performed separately by setting the degrees of freedom of the other joints to zero. In this way the
Table IV Analysis of variance with post hoc testing to compare the principal actlon In the three different positions Muscle DP DA PMCL SSP Abbrewotlons
Position
Position
l-2
l-3
Position
2-3
* * * * as in Table
* * I
*PC005
mechanical action of a multiarticular muscle such as the pectoralis muscle could be established with respect to each of the three joints that were involved (AC, SC, and GH joint).
RESULTS As can be concluded from Table II, the subjects were able to perform the requested task. The resultant force vector was in accordance with the target force vector in magnitude and in direction. Therefore the target force directions were used in the analysis and presentation of the data. The EMG results averaged over all subjects and all trials in position 1 (90” scapular abduction, forearm horizontal) are presented in Figure 2. Most curves show an asymmetric sinusoidal shape. A distinct EMG peak can be detected in a specific force direction. The force directions with low EMG levels are considered as the “silent” part of the curve. The three parts of the trapezius muscle (trapezius descending, trapezius transverse, and
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DA
DM EMG I” %
EMG in % 120
120,
I
-201, 0
45
90
135
160
225
270
316
360
/ 45
0
90
force darection (degrees)
135
160
force direction
, 225
270
315
8’ 360
. 315
r 360
315
360
(degrees)
DP EMG I” %
100 60 60 40 20 0 -20, 0
45
90
I,, 135
180
force directmn
225
1,, 270
315
360
(degrees)
PMCL
PMST EMG in %
EMG in % 120,
I
120rn
100
4
60
I
60 40 20 J\
0
-24 0
45
90
135
1.90
225
force direction
270
315
0
360
I 90
45
1 135
160
force direction
(degrees)
1 225
. 270
(degrees)
TM
LD
EMG in %
EMG in % 120
120
I
‘;J-J&
n -20’1
I 45
0
/ 90
I 135
I 160
I 225
force directm
Figure (abbrevlatlons
2
Electromyography/f as In Table
I 270
315
I’ 360
135
orce I)
160
force dwection
(degrees)
dIrectIon
curves
Error
bars
lndlcate
225
270
(degrees)
SD of elctromyography
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TD
TT EMG in %
EMG in %
120
force dreclton
(degrees)
TA
force dwction
(degrees)
force direction
(degrees)
SA EMG in %
EMG I” % 120,
I
0 -20 0
45
I 90
I 135
I 180
force dwctlon
225
270
315
I 360
(degrees)
IS
SSP EMG I” %
EMG in %
120
0
45
90
135
180
force dwction
225
270
315
360
(degrees)
ssc EMG in % 120
I
100
-r
0
45
90
135
180
force directmn
225
270
315
360
(degrees)
Figure
2
Cont’d
et al.
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366
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et al.
trapezius ascending) were mainly active in force directions varying from pointing upwards to an oblique directed force. The serratus anterior muscle was associated with an upward force direction. The pectoralis major muscle showed very distinct and clear peaks. For the clavicular part the principal action was between 270” and 315” and between 225” and 270” for the sternal part. The latissimus dorsi (LD) had a low EMG peak level in microvolts. As a consequence the EMG level in the silent part of the curve, expressed as a percentage of this peak, was relatively high. The teres maior muscle showed a principal action comparable to the LD but had a more distinctive peak. The principal action of this muscle was pointed downwards (135” to 180”). The deltoid muscle, consisting of three different force directions related to the orientation of these muscle parts. The three parts of the rotator cuff involved in this study behaved differently. The infraspinatus was active in a wide range of force directions. This resulted in a curve without a clear peak. Furthermore the individual subjects were inconsistent with respect to the principal action of the infraspinatus, as can be concluded from the large SD in Figure 2. The supraspinatus (SSP) was maximally activated in an upward force direction. The dual wire electrode of the SSP muscle malfunctioned in one subiect, as did the subscapularis (SSC) electrode in another subiect, probably because of direct contact between the wires. The activity of the SSC was maximal in a medially and downwards directed force. There was considerable interindividual variability. The teres minor was not included in this study. Table III shows the principal action in three different positions (1, 2, and 3) of 14 muscles averaged over all subjects and trials. To establish the influence of arm position on the principal action, analysis of variance with post hoc testing was performed (Table IV). The principal action of the anterior deltoid, the posterior deltoid, the pectoralis maior, and the SSP changed significantly (p -=c 0.05). The results of the mathematic shoulder model are summarized in Figure 3. The mechanical action is indicated by arrows. These arrows represent the force vectors in the force plane at the elbow that would result from a standardized contraction of each separate muscle or muscle part. The mechanical action is determined by the length and orientation of a muscle’s lever arm in relation to the joint. The length of the arrow is expressed in arbitrarv units.
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The relation between the mechanical action and the principal action indicates whether the observed muscle activation can be understood from the anatomic relations of the muscle (lever arm length and orientation). Most of the monoarticular muscles crossing the GH joint are maximally active in mechanically favorable force directions. This was the case for two of the rotator cuff muscles and the three parts of the deltoid. The mechanical action of the teres major differed 20” with the principal action. The EMG results of the SSC were not in harmony with the results obtained from the kinematic data. The principal action of the LD was in agreement with the mechanical action related to the SC joint. The principal action did not correspond with the mechanical action with respect to the AC and GH joints. The principal action of the two parts of the pectoralis muscle was approximately in harmony with the force directions that could be expected from the lever arms. The mechanical action of the serratus is difficult to interpret. The maximal EMG is seen in a force direction that equals the averaged mechanical action of the SC joint and the AC joint. Regarding the trapezius muscle there seems to be a clockwise shift when the model results are compared with the EMG results.
DISCUSSION EMG. For several
decades EMG has been used to estimate muscle force in the living human. It is important to realize that the EMG reflects the muscle force only to a limited extent. Studying the EMG results of shoulder muscles can be even more complicated. Normalization by means of reference contractions is a complex procedure, especially concerning the shoulder.27 Muscle length can change considerably during a normal abduction motion. This will have an important effect on the EMG results.*, I4 To avoid this problem we decided to use an isometric force task by varying the external force vector in a static position. Our point of interest was to detect the force vector that showed the highest EMG level (principal action) to get more insight in muscle function. Reference contractions were not necessary to establish the principal action. Cross talk is usually a problem in surface EMG. However, in contrast to the more classical approach, EMG level in microvolts was not important in our study; the principal action was only influenced by a neighboring muscle if it changed the force direction of maximal EMG. Any other influence such as in the absolute EMG level
1. Shoulder Elbow Volume 6, Number
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0’
downwards
dm
I
mochankal
180”
actlon
’
dp
tm
pmcl
et al.
0”
0” pmst
I
1800
Figure
3 Comparison between prlnclpal actlon and mechanlcal actIon In posItIon 1 Prlnclpal octlon (EMG data) IS represented by thick part of orcles (prlnclpal actlon averaged over subjects k SD, see Table III) MechanIcal action (model data of one of subiects) IS Indicated by arrows (length It- arbitrary units)
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et al.
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180'
IS
0'
1ao*
Figure
3 Cont’d
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J. Shoulder Elbow Surg. Volume 6, Number 4
or in the silent part of the curves caused no effect. Wire EMG proved to be a reliable method to monitor the muscle activity of muscles that are difficult to approach by means of surface EMG. Still, we have to bear in mind that wire EMG enables us to identify the activity of only a small muscle volume. We therefore advocate the use of surface EMG, if possible. For the less accessible SSC muscle we used the axillary approach as described by Nbmeth et al.15 In recent literature an alternative route is described, underneath the medial border of the scapula 4, ” which seems to be an attractive possibility to record the activity of the SSC in different parts of the muscle. Muscle function. Studying abduction movement will provide only limited insight in the function of shoulder muscles. This was first understood by Shevlin et al.23 and later by Bassett et al.2, Flanders and Soechting,5 and Pearl et al.18 However, only some aspects of these studies can be compared with our study, because the test position of the shoulder and the protocol were not the same. In our study the arm was suspended; no muscular force was necessary to keep the arm in the described positions. The resultant external moment with respect to the shoulder joint was comparable in all directions. In our opinion this is essential if polar plots of force or EMG are desired. Otis et al.16 demonstrated in an anatomic study that muscle lever arms depend on shoulder configuration. This finding is in agreement with our EMG results, as can be concluded from Table III and Table IV. The principal action is not a synonym for muscle function. It is therefore not correct to attribute one specific function to a shoulder muscle. Occasionally muscles show a synergistic way of contraction in one or more tasks. We could establish such a relationship for some muscles: the LD/teres major/SSP are activated simultaneously. In upward and slightly oblique force directions we observed activity in the trapezius, serratus, deltoid, and SSP. However, such synergistic patterns may be observed only in specific circumstances and tasks. Flanders and Soechting5 found a second peak in most of the shoulder muscles. A second peak could not be established in our results, possibly because of the limited number of data points. However, in our opinion it is difficult to distinguish these second peaks from artifacts such as cross talk or unneces-
Arwert
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369
sary cocontractions resulting from uncertainty of the subjects. In another recent EMG study of shoulder muscles’8 in which EMG level was also related to force direction, no second peak was observed. EMG and shoulder model. The mechanical action as calculated from the shoulder model was in harmony with the principal action in most of the shoulder muscles. This means that the muscle force (EMG) is applied efficiently in a favorable force direction. This observation was valid for the three parts of the deltoid muscle, for some of the multiartitular muscles, and for the SSP muscle. The rotator cuff muscles are usually associated with stabilization and not primarily with a contribution to external moment.4, lo, 13, 2o I n our study the observed principal action and the mechanical action of the SSC muscle were different. This result can be explained by assuming that the SSC has to be activated in a less optimal direction to secure glenohumeral stability or to compensate for unwanted forces from other muscles. The role of the infraspinatus muscle as a controlling and stabilizing muscle can be deduced from its continuous activation: this muscle was activated in all directions, as can be concluded from the large error bars in all directions and the absence of a distinct peak in Figure 2. Probably this muscle is important in prevention of stress on the passive structures of the GH joint in various external force directions. In medially and laterally directed forces the large multiarticular pectoralis major and LD muscles play an important role. The activation of these muscles has an effect on the SC joint, the AC joint, and the GH joint. Probably this explains why the subscapularis muscle has to be active in a relatively unfavorable direction-to tune and compensate unwanted side effects of the large pectoralis major and LD, which are spanning three joints. The thoracoscapular muscles (serratus and trapezius) have large lever arms as well, thereby offering stability for the scapula in upward and outward forces of the arm. As far as the trapezius muscle is concerned, we have to realize that the scapulothoracic gliding plane should also be considered a (nonsynovial) joint. The medial border of the scapula is always in contact with the thorax. Compressive forces can be expected there. The effect of this muscle with respect to this “joint” may cause the difference between the principal action and the mechanical action with respect to the SC and AC joints.
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13
Kronberg M, NCmeth G. Brostrom fi Muscle octlvlty and coordlnatlon In the normal shoulder An electromyographtc study Clan Orthop 1990,257 76-85
14
Ml&a GA Ergonomics
15
Nkmeth G, Kronberg M, Brostrom fi EMG recordings from the subscapulons muscle descrlptlon of o technique J Orthop Res I 990,8 15 l-3
16
Otis JC, Jlong CC, Wlcklewlcz Tl, Peterson MGE, Warren RF, Sontner TJ Changes In the momentorms of the rototor cuff and deltoid muscles with abduction and rotation J Bone Joint Surg Am 1994,76A 667-76
17
Pearl Ml, Perry J, Torburn 1, Gordon 1H An electromyogrophlc anolysls of the shoulder during cones ond planes of orm motion Presented at the Fifth Annual Meeting of the InternatIonal Conference on Surgery of the Shoulder, Porls, France, July 12-l 5, 1992
18
Peal1 Ml, Perry J, Torburn t, Gordon 1H An electromyographic anolysls of the shoulder during cones and planes of arm motion Cltn Orthop 1992,284 1 16-27
19
PerryJ, Bekey GA EMG-force relotlonshlps CRC Crlt Rev Blamed Eng 1981,7 l-22
20
Poppen NK, Walker PS Forces at the glenohumeral abductlon Clln Orthop 1978,135 165-70
21
Pronk GM A klnematlcol model of the shoulder J Med Eng Technol 1989,13 1 19-23
a r&urn&
22
Soha AK Dynamic stablllty of the glenohumeral Orthop Stand 197 1,42 49 l-505
lolnt
23
Harrymon II DT, SldlesJA, Horns St, Matsen II FA loxlty of the normal glenohumeral lolnt a o quantltlve In VIVO assessment J Shoulder Elbow Surg 1992,l 66-76
Shevltn MG, LehmonnJF, LUCCIJA Electromyographlc study of the functlon of some muscles crossing the glenohumerol lolnt Arch Phys Med Rehab 1969 264-70
24
Heckathorne CW, Chlldress DS RelatIonshIps of the surface electromyogram to the torte, length, velocity, and controctlon rate of the clneplastlc human biceps Am J Phys Med 198 1 , 60 l-19
Solomonow M, Boratta RV, D’Ambrosla R EMGforce relottons of a single skeletal muscle acting across a lolnt J Electromyogr Klneslol 199 1 , 1 58-67
25
Soslowsky geometry 181-90
P Blomechanlcal model of J Blomech 1987.20 157.
26
lnman VT, Sounders JB, Abbott LC Observations on the function of the shoulder lolnt J Bone Joint Surg Am 1944, 26A l-30
Van der Helm FCT, Veeger HEJ, Pronk GM, Van der Woude LHV, Rozendal RH Geometry parameters for musculoskeletal modelllng of the shoulder system J Blomech 1992,Z 129. 44
27
Van Woensel W, Arwert HJ Effects of external lood and abductlon angle on EMG level of shoulder muscles during lsometnc action Electromyogr Chn Neurophyslol 1993.3 185-91
28
Veeger HEJ, Von der Helm FCT, Van der Woude GM, Rozendol RH Inert10 and muscle contractton for musculoskeletol modelllng of the shoulder J Blomech 199 1,7 6 15-29
The principal action of the serratus anterior, crossing the SC joint and the AC joint, seems to be a compromise between the difference in mechanical action with respect to both joints. The authors thank Wire Dee enaars and Wit Meijer for their assistance in data co 7lection and processing, and Hans Fraterman for the technical realization and his general support.
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12
Keoting JF, Waterworth P, Show-Dunn relative strength of the rototor cuff muscles 1993 75B 137-40
J, Crossan J The J Bone Joint Surg Br
The quontlflcatlon 199 1,34 343-52
of EMG
LJ, Flotow El, BIglIon of the glenohumeral lolnt
normollzatlon
error
In skeletal
muscle lolnt In
Acta
lU, Mow VC Artlculor Clan Orthop 1992,285
LHV, Pronk parameters mechomsm
L M
muscles Van Woensel,
MSc,
In a static force task the electromyographic level of 74 shoulder muscles including 3 rotator cuff muscles was related to force direction. Surface and wire electrodes were used. The force direction of maximal electromyography (principal action) was identified for every muscle. The principal action expresses the function of a muscle in a specific situation. The deltoid was active in a force direction that could be understood from its anatomy. The trapezius and serrafus were main/y involved in stabilizing the scapula in upward and outward force directions. large multiarticular muscles such as the pectoralis and the latissimus were active in downward and forward forces. The rotator cuff seems to have a specific role in stabilizing the gienohumeral joint. These data can be compared with data of patients with shoulder disorders and with kinematic data of a shoulder model. (J SHOULDER E~5ow SURG
1997;6:360-70.1 Ttt e s h ou Id er is an interesting but complex mechanism. It enables us to position the arm and hand effectively in a three-dimensional working space. The shoulder consists of 3 bones, 17 muscles, and 3 joints 28.. the sternoclavicular (SC) joint, the acromioclavicular (AC) joint, and the glenohumeral (GH) joint. All three joints participate in any motion of the shoulder.‘O The underlying causes of some important shoulder disorders such as instability or impingement are still not fully understood. To reveal the cause of these shoulder disorders, more has to be known about the biomechanical and coordinative behavior of the normal shoulder and about the function of shoulder muscles. Recent publications show a growing interest in this subject.5, ‘, 9, 12, 13, la, 25, x The goals of our study included the following. (1) To describe muscle function of the shoulder. In general, electromyography (EMG) can be a useful method to study muscle function, although there
From the State University of leaden, Research Group of Kineslology, Department of Orthopedics, Delft Umvenlty of Technology, Laboratory of Measurement and Control, and AcademIcal Hosprtal of leaden, Department of Orthopedics Reprmt requests Henk J Arwert, MD, MSc, State Unlverslh/ of Leaden. Research Grout of Klnesloioav, Deoortment of Orthopedlcs, Rlinsburgelweg 10, 2333 AA”celden’, The Netherlands CopyrIght Board
0
105%2746/97/$5
360
1997
by Journal
of Shoulder
of Trustees 00 + 0
32/l/79906
ond
Elbow
Surgery
are some technique-related problems.3, 19, 24 (2) To determine to what extent we can derive muscle function from the orientation of a muscle’s lever arm with respect to the joint axis. The EMG results of our study were compared with a biomechanical shoulder model.21, 26, 28 (3) To test our hypothesis that muscle function can depend on shoulder position. We were interested in the relation between the function of shoulder muscles and the position of the shoulder joint. The lever arm of the subscapularis muscle, for example, depends on the position of the GH joint. Because of this, the subscapularis function might be influenced by humeral abduction.16 Special attention was paid to the function of the rotator cuff muscles. As assumed previous4, 6~ 13, 20, 22 indications were found that this IYI muscle group plays a specific role.
METHODS EMG. EMG
of 14 muscles or muscle groups was recorded in two sessions with the use of bipolar surface electrodes or intramuscular wires’, l5 (Table I). The surface electrodes had a fixed interelectrode distance of 21.5 mm. Electrode positions were standardized (Table I). The dual wire electrodes were made of Teflon-coated platinum (0.10 mm). The wires were not insulated at the tip (1 mm); the distance between the tips was 2 mm. The subjects were asked to move their
Atwert
1. Shoulder Elbow 5x-g. Volume 6, Number 4
Table I Muscles
Involved
Muscle
Electrode
DA DM
In this study and the type and posItion Electrode Middle
Surface Surface Surface
DP TD TT
of the muscle
4 cm above
TA
Surface
PMCL PMST
Surface Surface
SA
Surface
6th head
LD IS
Surface Surface
SSP ssc TM DA, Anterior ascending; dorsi, joint,
deltoid; PMCL,
Mlddle
spanned
AC,
the margin
of the muscle.
TS, an % of the line between
of the sternal
TS and
PS.
T8.
SC SC, AC SC, AC AC,
GH GH
6 cm below Al, lateral part Middle of the muscle belly
SC, AC, GH
GH
Wire Wire
Middle Axillar
GH
Surface
3 cm up and
SSP, supraspinatus; Ioint;
KS, scapular
below
part
GH
SC, AC, SC, AC
axillary
fold
of the muscle approach
DM, medial deltoid; DP, posterior pectoralis major, clavicular part,
IS, infrasplnatus, G/i, glenohumeral
Joints
belly
On % of the line between TS and Middle of the clavicular part
lateral
from
GH GH
Al
deltoid; JD, trapezius pectoralis malor,
PMSJ,
SSC, subscapularis; spine; KS, spinal
TM, teres process;
361
of the electrodes
location
Middle of the muscle belly Middle of the muscle belly Right above TS, 2 cm below
Surface Surface
et al.
descending; pars sternal
major; A/, inferior
77, trapezius, transverse; part; SA, serratus anterior,
SC, sternoclavicular angle; MM, medial
joint; AC, margin;
JA, trapezius, ID, latissimus
acromioclavicular J8, eighth thoracic
vertebra.
shoulder as little as possible after insertion of the wires to avoid wrinkling or breakage of the wires. If, however, some scapular motion occurred, the wires slid in and out without wrinkling. Discomfort caused by the wires was minimal once the wires were inserted. At the end of the recording session the wires were removed and checked; no breakage was observed. The EMG signal was preamplified, high-passfiltered (10 Hz), amplified, and stored on tape. Before AD conversion (1000 Hz, 12 bit) an analog low-pass filter (500 Hz) was used. All measurements were performed on the right shoulder. Experimental setup. Five healthy subjects participated in this study (mean age 26 years, 1 man, 4 women). Twelve muscles were recorded in the first session. The subjects were seated in three different positions. Position 1 was 90” scapular abduction, the elbow in a 90” flexed orthosis, and the forearm horizontal. Position 2 was 90” anteflexion of the humerus, the elbow in a 90” flexed orthosis, and the forearm vertical (Figure 1). Position 3 was 90” of anteflexion of the humerus, the elbow in a 90” flexed orthosis, and the forearm horizontal. In the second session we collected the data of two other muscles (teres maior, pectoralis major, sternal portion) in three of the subjects in position 1. A local coordinate system (xyz) was used for the humerus. The y axis was in line with the humeral shaft. The z axis was parallel to the forearm. The x
axis was perpendicular with respect to the y axis and the z axis. A positive moment around the z axis in position 1 and 3 led to a force directed downwards and in position 2 to a medially directed force. A support was provided for the subiect’s head and back. The elbow orthosis was suspended to compensate for gravity. This enabled the subjects to relax their arm in any of the three positions. The elbow orthosis was connected with a strain-gauge two-dimensional force transducer. The two-dimensional force plane was perpendicular to the humerus. This force transducer registrated forces in the x- and z-direction. The subjects were visually informed by means of a monitor about the force vector they exerted (force level and direction). This resultant force vector was digitized and compared with the target force vector that was shown on the monitor. It is important to note that the subjects were not restricted or constrained in humeral axial rotation or backward-forward translations, so the force vector was always perpendicular to the humerus. Because the arm was suspended, no muscle activity was needed to keep the arm in position. Procedure. First, the subjects were asked to relax their shoulder muscles. This was controlled by the EMG. Subsequently the force transducer was set to zero by removing the offset in the x and z directions. Subjects were asked to exert a force in eight alternating directions in the force plane (per-
362
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et al.
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SO
Figure and
Table
actual
1 ExperImental force
vector
setup were
II Resultant force directions
Subjects
direction (‘I
0 45
90 135 180 225 270 315 Mean resultant force (N)
able
to see monitor
and force levels averaged Position
Target
were
Resultant direction
On
momtor,
target
force
vector
displayed
(“)
0.9 46.4 90 6 135.3 181.4 224 9 271 3 315 1 140
1
over five sublects, Position
SD
0.8 0.7 0.5 03 0.4 1.3 0.6 1.0 0.2
Resultant direction
0.2 46.5 90.4 135.6 181.3 225.1 270.3 315.4 139
(“)
2
presented
for each Position
SD
0.5 0.8 07 0.5 0.4 12 09 10 03
Resultant direction
0.9 45.4 89.9 135.5 181.2 225.0 269.9 315.5 14.0
(‘)
posltton
3
SD
0.5 0.5 0.6 04 0.4 0.6 0.5 05 07
Target force level was 14 N in every direction.
pendicular to the humerus) without changing their position. The resultant force vector was displayed on the monitor. The task was to aim this vector at one of the displayed targets and to maintain this force for 3 seconds. Eight force directions were studied: 0” (upwards) and clockwise steps of 45”; 90” was directed laterally, 270” medially (Figure 1). The target force level was 14 N in all directions (compensated for gravity). A period of at least 1 second was selected, during which the resultant force vector was constant in magnitude and direc-
tion. The EMG signal was rectified and averaged. One trial consisted of eight alternating force directions; every subject performed three trials in every position. In every trial the highest EMG value of a muscle was set to 100%. The subjects had to practice three trials to become familiar with the force task. Data processing and interpretation. The force direction in which the EMG of a specific muscle was maximal was one of the most important parameters that could be obtained from the EMG
1. Shoulder Elbow Volume 6, Number
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Table III Descriptive
statistics of the prlnclpal Position
Muscle
Mean 339 21 74 0 56 56 276 260 333 143 34 356 151 149
DA DM DP TD Tr TA PMCL PMST SA LD IS SSP ssc TM Abbreviations
as in Table
action
(In degrees)
1
Position SD 16.3 198 13.6
245 96 14.0 11.0
3.8 66 206 666 28 7 309 10.3
Mean
obtalned
Position
2 Mean
8.0 13.5 18.2 10.2 173 140 9.8 9.2 12.7 28.3 246 31.2
341 127 80 51 171
363
by electromyography
SD
354 20 108 0 70 65 293
et al.
3 SD
333 26 92 9 68 58 290 325 128 68 40 146 -
130 21 2 9.2 25.8 15.3 13.6 10.3 12.0 55 566 307 33.2
I
data. This parameter is called the principal action.17 The principal action was estimated by means of a curve fitting procedure. This was done by applying a second order polynomial fit to the data points that constitute the peak in the EMG/ force direction curves. The principal action is not influenced by normalization methods. We used a kinematic analysis by means of a biomechanical shoulder model that is described in detail by Prank*’ and by Van der Helm et al.26 This three-dimensional model is based on the dissection of cadaver shoulders and consists of 3 joints, 3 ligaments, and 95 muscle elements. This model needs the digitized three-dimensional configuration of the shoulder girdle as input parameters. The procedure to obtain these coordinates is described by Prank.*’ We compared the principal action of each muscle with its mechanical action. The mechanical action was defined as the force vector in the plane of the force transducer that would result from a standardized force of one specific muscle. This standardized force was not related to the crosssectional area or muscle architecture; the mechanical action depends only on the muscle lever arm with respect to a specific joint. This procedure was performed for one of the subjects in position 1, After the bony landmarks of the shoulder were digitized, the model was provided with the necessary parameters to calculate the mechanical action. For every joint these calculations were performed separately by setting the degrees of freedom of the other joints to zero. In this way the
Table IV Analysis of variance with post hoc testing to compare the principal actlon In the three different positions Muscle DP DA PMCL SSP Abbrewotlons
Position
Position
l-2
l-3
Position
2-3
* * * * as in Table
* * I
*PC005
mechanical action of a multiarticular muscle such as the pectoralis muscle could be established with respect to each of the three joints that were involved (AC, SC, and GH joint).
RESULTS As can be concluded from Table II, the subjects were able to perform the requested task. The resultant force vector was in accordance with the target force vector in magnitude and in direction. Therefore the target force directions were used in the analysis and presentation of the data. The EMG results averaged over all subjects and all trials in position 1 (90” scapular abduction, forearm horizontal) are presented in Figure 2. Most curves show an asymmetric sinusoidal shape. A distinct EMG peak can be detected in a specific force direction. The force directions with low EMG levels are considered as the “silent” part of the curve. The three parts of the trapezius muscle (trapezius descending, trapezius transverse, and
364
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J. Shoulder Elbow July/August
DA
DM EMG I” %
EMG in % 120
120,
I
-201, 0
45
90
135
160
225
270
316
360
/ 45
0
90
force darection (degrees)
135
160
force direction
, 225
270
315
8’ 360
. 315
r 360
315
360
(degrees)
DP EMG I” %
100 60 60 40 20 0 -20, 0
45
90
I,, 135
180
force directmn
225
1,, 270
315
360
(degrees)
PMCL
PMST EMG in %
EMG in % 120,
I
120rn
100
4
60
I
60 40 20 J\
0
-24 0
45
90
135
1.90
225
force direction
270
315
0
360
I 90
45
1 135
160
force direction
(degrees)
1 225
. 270
(degrees)
TM
LD
EMG in %
EMG in % 120
120
I
‘;J-J&
n -20’1
I 45
0
/ 90
I 135
I 160
I 225
force directm
Figure (abbrevlatlons
2
Electromyography/f as In Table
I 270
315
I’ 360
135
orce I)
160
force dwection
(degrees)
dIrectIon
curves
Error
bars
lndlcate
225
270
(degrees)
SD of elctromyography
h-g. I997
I. Shoulder Volume 6,
E/bow Number
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Surg. 4
TD
TT EMG in %
EMG in %
120
force dreclton
(degrees)
TA
force dwction
(degrees)
force direction
(degrees)
SA EMG in %
EMG I” % 120,
I
0 -20 0
45
I 90
I 135
I 180
force dwctlon
225
270
315
I 360
(degrees)
IS
SSP EMG I” %
EMG in %
120
0
45
90
135
180
force dwction
225
270
315
360
(degrees)
ssc EMG in % 120
I
100
-r
0
45
90
135
180
force directmn
225
270
315
360
(degrees)
Figure
2
Cont’d
et al.
365
366
Arwert
et al.
trapezius ascending) were mainly active in force directions varying from pointing upwards to an oblique directed force. The serratus anterior muscle was associated with an upward force direction. The pectoralis major muscle showed very distinct and clear peaks. For the clavicular part the principal action was between 270” and 315” and between 225” and 270” for the sternal part. The latissimus dorsi (LD) had a low EMG peak level in microvolts. As a consequence the EMG level in the silent part of the curve, expressed as a percentage of this peak, was relatively high. The teres maior muscle showed a principal action comparable to the LD but had a more distinctive peak. The principal action of this muscle was pointed downwards (135” to 180”). The deltoid muscle, consisting of three different force directions related to the orientation of these muscle parts. The three parts of the rotator cuff involved in this study behaved differently. The infraspinatus was active in a wide range of force directions. This resulted in a curve without a clear peak. Furthermore the individual subjects were inconsistent with respect to the principal action of the infraspinatus, as can be concluded from the large SD in Figure 2. The supraspinatus (SSP) was maximally activated in an upward force direction. The dual wire electrode of the SSP muscle malfunctioned in one subiect, as did the subscapularis (SSC) electrode in another subiect, probably because of direct contact between the wires. The activity of the SSC was maximal in a medially and downwards directed force. There was considerable interindividual variability. The teres minor was not included in this study. Table III shows the principal action in three different positions (1, 2, and 3) of 14 muscles averaged over all subjects and trials. To establish the influence of arm position on the principal action, analysis of variance with post hoc testing was performed (Table IV). The principal action of the anterior deltoid, the posterior deltoid, the pectoralis maior, and the SSP changed significantly (p -=c 0.05). The results of the mathematic shoulder model are summarized in Figure 3. The mechanical action is indicated by arrows. These arrows represent the force vectors in the force plane at the elbow that would result from a standardized contraction of each separate muscle or muscle part. The mechanical action is determined by the length and orientation of a muscle’s lever arm in relation to the joint. The length of the arrow is expressed in arbitrarv units.
J. Shoulder Elbow July/August
Surg. I997
The relation between the mechanical action and the principal action indicates whether the observed muscle activation can be understood from the anatomic relations of the muscle (lever arm length and orientation). Most of the monoarticular muscles crossing the GH joint are maximally active in mechanically favorable force directions. This was the case for two of the rotator cuff muscles and the three parts of the deltoid. The mechanical action of the teres major differed 20” with the principal action. The EMG results of the SSC were not in harmony with the results obtained from the kinematic data. The principal action of the LD was in agreement with the mechanical action related to the SC joint. The principal action did not correspond with the mechanical action with respect to the AC and GH joints. The principal action of the two parts of the pectoralis muscle was approximately in harmony with the force directions that could be expected from the lever arms. The mechanical action of the serratus is difficult to interpret. The maximal EMG is seen in a force direction that equals the averaged mechanical action of the SC joint and the AC joint. Regarding the trapezius muscle there seems to be a clockwise shift when the model results are compared with the EMG results.
DISCUSSION EMG. For several
decades EMG has been used to estimate muscle force in the living human. It is important to realize that the EMG reflects the muscle force only to a limited extent. Studying the EMG results of shoulder muscles can be even more complicated. Normalization by means of reference contractions is a complex procedure, especially concerning the shoulder.27 Muscle length can change considerably during a normal abduction motion. This will have an important effect on the EMG results.*, I4 To avoid this problem we decided to use an isometric force task by varying the external force vector in a static position. Our point of interest was to detect the force vector that showed the highest EMG level (principal action) to get more insight in muscle function. Reference contractions were not necessary to establish the principal action. Cross talk is usually a problem in surface EMG. However, in contrast to the more classical approach, EMG level in microvolts was not important in our study; the principal action was only influenced by a neighboring muscle if it changed the force direction of maximal EMG. Any other influence such as in the absolute EMG level
1. Shoulder Elbow Volume 6, Number
da
Arwert
Surg. 4
0’
downwards
dm
I
mochankal
180”
actlon
’
dp
tm
pmcl
et al.
0”
0” pmst
I
1800
Figure
3 Comparison between prlnclpal actlon and mechanlcal actIon In posItIon 1 Prlnclpal octlon (EMG data) IS represented by thick part of orcles (prlnclpal actlon averaged over subjects k SD, see Table III) MechanIcal action (model data of one of subiects) IS Indicated by arrows (length It- arbitrary units)
367
36%
Arwert
et al.
J. Shoulder
Elbow
July/August
I
180'
IS
0'
1ao*
Figure
3 Cont’d
Surg. I997
J. Shoulder Elbow Surg. Volume 6, Number 4
or in the silent part of the curves caused no effect. Wire EMG proved to be a reliable method to monitor the muscle activity of muscles that are difficult to approach by means of surface EMG. Still, we have to bear in mind that wire EMG enables us to identify the activity of only a small muscle volume. We therefore advocate the use of surface EMG, if possible. For the less accessible SSC muscle we used the axillary approach as described by Nbmeth et al.15 In recent literature an alternative route is described, underneath the medial border of the scapula 4, ” which seems to be an attractive possibility to record the activity of the SSC in different parts of the muscle. Muscle function. Studying abduction movement will provide only limited insight in the function of shoulder muscles. This was first understood by Shevlin et al.23 and later by Bassett et al.2, Flanders and Soechting,5 and Pearl et al.18 However, only some aspects of these studies can be compared with our study, because the test position of the shoulder and the protocol were not the same. In our study the arm was suspended; no muscular force was necessary to keep the arm in the described positions. The resultant external moment with respect to the shoulder joint was comparable in all directions. In our opinion this is essential if polar plots of force or EMG are desired. Otis et al.16 demonstrated in an anatomic study that muscle lever arms depend on shoulder configuration. This finding is in agreement with our EMG results, as can be concluded from Table III and Table IV. The principal action is not a synonym for muscle function. It is therefore not correct to attribute one specific function to a shoulder muscle. Occasionally muscles show a synergistic way of contraction in one or more tasks. We could establish such a relationship for some muscles: the LD/teres major/SSP are activated simultaneously. In upward and slightly oblique force directions we observed activity in the trapezius, serratus, deltoid, and SSP. However, such synergistic patterns may be observed only in specific circumstances and tasks. Flanders and Soechting5 found a second peak in most of the shoulder muscles. A second peak could not be established in our results, possibly because of the limited number of data points. However, in our opinion it is difficult to distinguish these second peaks from artifacts such as cross talk or unneces-
Arwert
et al.
369
sary cocontractions resulting from uncertainty of the subjects. In another recent EMG study of shoulder muscles’8 in which EMG level was also related to force direction, no second peak was observed. EMG and shoulder model. The mechanical action as calculated from the shoulder model was in harmony with the principal action in most of the shoulder muscles. This means that the muscle force (EMG) is applied efficiently in a favorable force direction. This observation was valid for the three parts of the deltoid muscle, for some of the multiartitular muscles, and for the SSP muscle. The rotator cuff muscles are usually associated with stabilization and not primarily with a contribution to external moment.4, lo, 13, 2o I n our study the observed principal action and the mechanical action of the SSC muscle were different. This result can be explained by assuming that the SSC has to be activated in a less optimal direction to secure glenohumeral stability or to compensate for unwanted forces from other muscles. The role of the infraspinatus muscle as a controlling and stabilizing muscle can be deduced from its continuous activation: this muscle was activated in all directions, as can be concluded from the large error bars in all directions and the absence of a distinct peak in Figure 2. Probably this muscle is important in prevention of stress on the passive structures of the GH joint in various external force directions. In medially and laterally directed forces the large multiarticular pectoralis major and LD muscles play an important role. The activation of these muscles has an effect on the SC joint, the AC joint, and the GH joint. Probably this explains why the subscapularis muscle has to be active in a relatively unfavorable direction-to tune and compensate unwanted side effects of the large pectoralis major and LD, which are spanning three joints. The thoracoscapular muscles (serratus and trapezius) have large lever arms as well, thereby offering stability for the scapula in upward and outward forces of the arm. As far as the trapezius muscle is concerned, we have to realize that the scapulothoracic gliding plane should also be considered a (nonsynovial) joint. The medial border of the scapula is always in contact with the thorax. Compressive forces can be expected there. The effect of this muscle with respect to this “joint” may cause the difference between the principal action and the mechanical action with respect to the SC and AC joints.
370
Arwert
et al.
J. Shoulder Elbow July/August
13
Kronberg M, NCmeth G. Brostrom fi Muscle octlvlty and coordlnatlon In the normal shoulder An electromyographtc study Clan Orthop 1990,257 76-85
14
Ml&a GA Ergonomics
15
Nkmeth G, Kronberg M, Brostrom fi EMG recordings from the subscapulons muscle descrlptlon of o technique J Orthop Res I 990,8 15 l-3
16
Otis JC, Jlong CC, Wlcklewlcz Tl, Peterson MGE, Warren RF, Sontner TJ Changes In the momentorms of the rototor cuff and deltoid muscles with abduction and rotation J Bone Joint Surg Am 1994,76A 667-76
17
Pearl Ml, Perry J, Torburn 1, Gordon 1H An electromyogrophlc anolysls of the shoulder during cones ond planes of orm motion Presented at the Fifth Annual Meeting of the InternatIonal Conference on Surgery of the Shoulder, Porls, France, July 12-l 5, 1992
18
Peal1 Ml, Perry J, Torburn t, Gordon 1H An electromyographic anolysls of the shoulder during cones and planes of arm motion Cltn Orthop 1992,284 1 16-27
19
PerryJ, Bekey GA EMG-force relotlonshlps CRC Crlt Rev Blamed Eng 1981,7 l-22
20
Poppen NK, Walker PS Forces at the glenohumeral abductlon Clln Orthop 1978,135 165-70
21
Pronk GM A klnematlcol model of the shoulder J Med Eng Technol 1989,13 1 19-23
a r&urn&
22
Soha AK Dynamic stablllty of the glenohumeral Orthop Stand 197 1,42 49 l-505
lolnt
23
Harrymon II DT, SldlesJA, Horns St, Matsen II FA loxlty of the normal glenohumeral lolnt a o quantltlve In VIVO assessment J Shoulder Elbow Surg 1992,l 66-76
Shevltn MG, LehmonnJF, LUCCIJA Electromyographlc study of the functlon of some muscles crossing the glenohumerol lolnt Arch Phys Med Rehab 1969 264-70
24
Heckathorne CW, Chlldress DS RelatIonshIps of the surface electromyogram to the torte, length, velocity, and controctlon rate of the clneplastlc human biceps Am J Phys Med 198 1 , 60 l-19
Solomonow M, Boratta RV, D’Ambrosla R EMGforce relottons of a single skeletal muscle acting across a lolnt J Electromyogr Klneslol 199 1 , 1 58-67
25
Soslowsky geometry 181-90
P Blomechanlcal model of J Blomech 1987.20 157.
26
lnman VT, Sounders JB, Abbott LC Observations on the function of the shoulder lolnt J Bone Joint Surg Am 1944, 26A l-30
Van der Helm FCT, Veeger HEJ, Pronk GM, Van der Woude LHV, Rozendal RH Geometry parameters for musculoskeletal modelllng of the shoulder system J Blomech 1992,Z 129. 44
27
Van Woensel W, Arwert HJ Effects of external lood and abductlon angle on EMG level of shoulder muscles during lsometnc action Electromyogr Chn Neurophyslol 1993.3 185-91
28
Veeger HEJ, Von der Helm FCT, Van der Woude GM, Rozendol RH Inert10 and muscle contractton for musculoskeletol modelllng of the shoulder J Blomech 199 1,7 6 15-29
The principal action of the serratus anterior, crossing the SC joint and the AC joint, seems to be a compromise between the difference in mechanical action with respect to both joints. The authors thank Wire Dee enaars and Wit Meijer for their assistance in data co 7lection and processing, and Hans Fraterman for the technical realization and his general support.
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