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Journal of Orthopaedic Research 19 (1001) 206-212
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Dynamic contributions to superior shoulder stability
A.M. Halder, K.D. Zhao, S.W. O'Driscoll, B.F. Morrey, K.N. An *
h f a j o Clinic, Orthopedic Biamechanic~Lahouatory, ,700 First Street S U', Rochrster, hfN 5590.5, LISA
Received 1 November 1999; accepted 24 April 2000
Abstract
It has been suggested that superior decentralization of the humeral head is a mechanical factor in the etiology of degenerative
rotator cuff tears. This superior decentralization may be caused by muscular imbalance. The objective of this study was to investigate
the contribution of individual shoulder muscles to superior stability of the glenohumeral joint. In 10 fresh frozen cadaver shoulders
the tendons of the rotator cuff, teres major, latissimus, pectoralis major, deltoid and biceps were prepared. The shoulders were tested
in a shoulder-loading device in O", 30°, 60" and 90" of glenohumeral abduction. A constant superior force of 20 N was applied to the
humerus. Tensile loads were applied sequentially to the tendons in proportion to their cross-sectional areas and translations of the
humeral head relative to the glenoid were recorded with a 3Space'" Fastrak system. Depression of the humeral head was most
effectively achieved by the latissimus (5.6 f 2.2 mm) and the teres major (5.1 k 2.0 mm). Further studies should elucidate their
possible in vivo role in the frontal plane force couple to counter balance the deltoid. The infraspinatus (4.6 i2.0 mm) and subscapularis (4.7 i 1.9 mm) showed similar effects while the supraspinatus (2.0 & 1.4 mm) was less effective in depression. Therefore,
the infraspinatus and subscapularis should be surgically repaired whenever possible. The supraspinatus may be of less importance
for superior stability than previously assumed. Published by Elsevier Science Ltd on behalf of Orthopaedic Research Society.
Introduction
Rotator cuff lesions are among the most common
shoulder diseases. However, the origin of rotator cuff
degeneration is still unclear. Possible explanations include intrinsic factors such as decreased circulation in
the critical area with limited vascularization [29] or
changes in collagen synthesis and turnover [30]. Extrinsic factors include increased shear and compressive
forces as a result of a narrowed acromio-humeral interval [24,31]. It is probable that a combination of intrinsic and extrinsic factors is present prior to rotator
cuff failure [32].
A decrease in acromio-humeral distance may be due
to osteophytes on the undersurface of the acromion or
hypertrophy of the coracoacromial ligament [ 1,9,22], as
well as superior migration of the humeral head
[7,34,31,391. Superior decentralization of the humeral
head may increase shear and compressive forces on the
rotator cuff tendons. This potentially causes fiber dis-
*Corresponding author. Tel.:
+ 1-507-281-2262;fax: + 1-507-284-
5392.
E-ma2 address: aii.kainan(a~mayo.edu
(K.N. An).
ruption on the bursa1 and articular side [21], as well as
sclerosis of the acromion and thickening of the coracoacromial ligament [4]. This would further narrow the
acromio-humeral interval initiating a vicious cycle
eventually leading to rotator cuff rupture. However,
superior decentralization of the humeral head may be
the cause as well as the result of rotator cuff thinning.
Several studies identified static structures contributing to superior stability of the glenohumeral joint. In
conjunction with the insertion of the long head of biceps
tendon. the glenoid labrum has a stabilizing effect [26].
The size of the rotator cuff interval also seems to be
important [ 131. Negative intraarticular pressure has a
stabilizing effect in all directions but only at low loads
~141.
Few studies have focused on dynamic stabilizers of
the glenohumeral joint in the superior-inferior direction
[6,11,24,31.34,37]. Their results are controversial and the
relative contributions to superior stability of different
shoulder muscles are not yet known. However, this
would be of tremendous importance in order to address
the most effective muscles in conservative treatment of
the impingement syndrome as well as postoperative rehabiliation. Furthermore, it would help to direct rotator
cuff surgery to the most relevant structures. The objective of this study was to investigate the contribution of
0736-0266/01/$ - see front matter Published by Elsevier Science Ltd on behalf of Orthopaedic Research Society.
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A. hf. Hulder rt al. I Journal of'Orthopaedic Rrsrurch 19 (2001) 206-212
different muscles to superior gelnohumeral stability.
These contributions may be relevant to our understanding of the etiology and prevention of rotator cuff
degeneration.
Materials and methods
Ten fresh frozen cadaver shoulders without rotator cuff tears or
radiological evidence of glenohumeral osteoarthritis were used in the
study. During dissection, preparation and testing the specimens were
moistened using physiologic saline solution to prevent dehydration. All
soft tissues superficial to the muscles were removed except rotator cuff
muscles, teres major, latissimus, deltoid and pectoralis major muscles
and their respective tendons. All muscles, except the deltoid, were elevated from the bone and resected at the musculotendinous junction.
The deltoid was preserved. Their tendons were carefully separated
from surrounding soft tissue to ensure unrestricted movement. Nylon
strings were sutured to each margin of the flat tendons to allow even
loading. Fiberglass rods were cemented into the medullary canals of
the proximal humeri to control position in the frontal plane. Thinner
rods were fixed in drill holes perpendicular to the humeral shaft in the
neutral position employing the bicipital groove as a landmark to
control rotation. The scapulae were mounted onto a Plexiglas plate.
The shoulder-testing device (Fig. 1) was made of non-metal materials to avoid interference with the electromagnetic tracking device. A
hinged Plexiglas are attached to the humerus allowed control of the
degree of abduction. Through variable-position pulleys, strings from
the tendons were connected to pneumatic actuators (Airpot Corporation, Norwalk, Connecticut, USA). A commercially-available computer controlled by Labview'" software (National Instruments
Corporation 1994, Austin, Texas, USA) drove electro-pneumatic
valves (Proportion-Air 1997, McCordsville, Indiana, USA) to load the
pneumatic actuators. Custom-made load cells on each cylinder verified
the applied loads. A 3Space'" Fastrak system (Polhemus 1993, Col-
207
Chester, Vermont, USA) measured the three-dimensional positions and
orientations of sensors attached to the specimen in relation to the
source of electromagnetic waves.
The glenohumeral joint was positioned according to laser-pointers
which were located superiorly and laterally and whose beam intersected at the center of rotation of the hinged arc. The scapulae were
aligned and rigidly mounted in the shoulder-testing device so that the
medial margin of the scapula was in line with the vertical axis of the
device, and the humeral head was in the center of the pivoting arc.
Nylon loops were sutured to the tendons and were connected to the
pneumatic actuators by strings that were guided by pulleys. The positions of the pulleys were carefully adjusted so that the strings imitated
muscle lines of action by running through the centroids of each muscle
[16]. Finally, 3Space'" sensors were attached to the proximal humerus
close to the head and to the spine of the scapula. The source of the
electromagnetic waves was rigidly mounted in line with the vertical
axis of the shoulder-testing device.
To selectively investigate the stabilizing function of the tested
muscles only translations of the humeral head relative to the glenoid
were allowed while the humerus was kept in a fixed degree of abduction in the scapular plane. As tightness of the ligaments in the extremes
of motion kept in the muscles from generating vertical translations
[13,38] the humerus was locked in neutral rotation. The experiment
started in the hanging arm position and was performed in 30", 60". and
90" of glenohumeral abduction (Fig. 2). The joints were confirmed to
be vented prior to testing. Of the muscles tested, the pectoralis major
and the latissimus did not originate from the scapula. Therefore, adjusting the pulleys according to the scapular tilt [28] changed their lines
of action.
The potentials of different muscles to reverse superior translation of
the humeral head were measured. Superior translation of the humeral
head was accomplished by application of a constant superior force of
20 N. The depressor effects of the supraspinatus, infraspinatus, teres
minor, teres major, latissimus, superior and inferior part of the subscapularis, pectoralis major, and long head of biceps were tested. The
tendons were loaded sequentially in random order in line of muscle
action and proportional to their respectivc physiologic cross-sectional
Pulley
Actuator
Weight
Actuator
Control
System
Fig. 1. Shoulder testing device. A hinged Plexiglas arc attached to the humerus allowed control of abduction and rotation. Strings from the tendons
were connected to pneumatic actuators through pulleys that were variable in position. A commerically-available computer drove electropneumatic
valves to load the pneumatic actuators. Custom-made load cells on each cylinder verified the applied loads. A 3Space'" Fastrak system attached to
the specimen measured the three-dimensional positions and orientation of sensors in relation to the source of electromagnetic waves.
A.M. Hulder et ul. I Journul
of
Orthopurdic Rescurch 19 (2001) 206-212
3-Space Sensor
Humerus
3-Space Sensor
Scapula
Pulley
String
3-Space Sensor
Ninged Arc
Pulley
Weight
Actuator
Fig. 2. Testing of the infraspinatus muscle in the hanging arm position. The humertls was locked in neutral rotation. A constant superior force of 20 N
was applied to the humerus, and the tendon was loaded in line of muscle action proportional to its cross-sectional area by computer-controlled
pneumatic actuators. Positional measurements were taken by a 3Space'" Fastrak system.
areas (reported hy Veeger [36]). This was based on the assumption that
the maximum generated muscle force is proportional to its cross-sectional area [35].To ensure identical starting positions for all muscles,
the humerus was reset between each test according to position values
provided by the 3Space'" Fastrak system. After testing, the glenohumeral joint was disarticulated. and the bony landmarks were digitized
to determine their positions relative to Ihe sensors.
From the digitization data, the center of the humeral head, defined
as the geometric center of its convexity, and the center of the glenoid,
defined as the intersection of its vertical and horizontal axes, were
calculated. Translations caused by each muscle were calculated by
comparing the positions of the center of the humeral head before and
after muscle loading. Results are reported as translation values in
millimeters for each joint position and as an average of all positions.
Summary statistics are reported as means ( M . D . ) .Translational
distances were lirst analyzed using two-factor analysis of variance with
repeated measures o n both [actors (muscle and arm position). However, because significant interactions between muscle and arm positions were identified, separate one-way repeated measures ANOVAs
were run for each arm position. Significant effects were then, further
analyzed using the Studeiit-Newman Keuls multiple comparison
procedure. All statistical tests were two-sided, with the threshold of
significance set at c( = 0.05. All analysis were performed using SAS
version 6.17 (SAS Institute, Cary, NC) on a Sun Ultra IT computer
(Sun Microsystems, Palo Alto, CA).
Results
Generally the largest translations were generated by
the tested muscles in 30" and 60" of glenohumeral abduction (Fig. 3). In the hanging arm position, the
translations were smaller because the superior joint
capsule limited inferior translations [13]. In 90" of
glenohumeral abduction the smallest translations oc-
curred because of the progressive tightness of the inferior glenohumeral ligament complex [25].
The latissimus was the most effective depressor (average: 5.6 i2.2 mm) which was significant (Table 1) in
the hanging arm position (5.5 i 1.0 mm). At 30"
( 7 . 6 f 3 . 0 mm), 60" (5.6+ 1.8 mm) and 90" (3.6%2.0
mm) of glenohumeral abduction, it was still significantly
( P < 0.05) more effective than all muscles tested, except
the teres major, the infraspinatus and the subscapularis.
In these positions, it had the most inferiorly directed line
of action, and its large cross-sectional area was capable
of generating high muscle force. With increasing abduction, the line of action of the latissimus became
perpendicular to the glenoid due to scapular tilt and
thus, became a compressor more than a depressor of the
humeral head.
The teres major was the second most effective depressor (average: 5.1 f 2.0 mm). Its inferiorly directed
line of action was constant in relation to the glenohumeral joint because it originated from the scapula and it
had a large cross-sectional area. It was significantly less
effective than the latissimus in the hanging arm position
(3.9 i 1.2 mm), but not significantly diffcrent from the
latissimus in 30" (6.9 i 1.7 mm), 60" (5.5 & 1.8 mm) and
90" (4.2 f 2.0 mm) of glenohumeral abduction.
The depressor effects of the infraspinatus (average:
4.6 f 3.0 mm) and subscapularis (average: 4.7 1.9 mm)
were comparable as their lines of action were similar.
Both were significantly ( P < 0.05) more effective than
*
A.M. Halder et al. I Journal of Orthopuedic Research 19 (2001i 206-212
209
Humeral Head Depressor Effects
hanging arm position
-g
30 degrees abduction R 60 degrees abduction
90 degrees abduction
10.0
I
8.0
v
2
6.0
3
B
5
4.0
G
ru
0
E
.3
2.0
m
v1
2
0.0
-2.0
muscle
Fig. 3. Translation values of the tested muscles in millimeters in hanging arm position, at 30", at 60" and at 90" of glenohumeral abduction. The
graphs depict the inferior translations of the humeral head relative to the glenoid effected by the tested muscles counteracting a constant superior
force of 20 N.
Table 1
The multiple comparisons test results using the Studen-NewmanKeuls procedure"
Muscle
Hanging arm
30"
60"
90"
Latissimus
A
A
A
A
Long head of biceps
B
BC
BC
B
Teres major
B
AB
A
A
Infraspinatus
BC
AB
AB
A
C
AB
AB
A
Subscapularis
Subscapularis inferior
C
BC
ABC A
Pectoralis major
E
B
D
D
Subscapularis superior
DE
C
C
B
Teres minor
DE
D
D
B
Supraspinat us
E
D
D
B
"Within each position, muscles with letters in common were not found
to be significantly different ( P > 0.05) in terms of their mean translational distance. Examination of this table shows the interaction between muscle and position.
the supraspinatus throughout all positions. The separately tested inferior portion of the subscapularis
generated significantly ( P < 0.05) larger inferior translations than the superior portion in the hanging arm
position and at 90" of glenohumeral abduction.
Probably due to its smaller cross-sectional area, the
teres minor was significantly ( P < 0.05) less effective in
depression (average: 2.3 f 1.2 mm) than the inferior
portion of the subscapularis.
The long head of biceps was comparable in depression (average: 4.0 It 2.1 mm) to the infraspinatus and
subscapularis in 30" (6.0 f 1.9 mm) and 60" (4.3 f 1.8
mm) of glenohumeral abduction but was less effective
than both in 90" of glenohumeral abduction (1.7 f
1.0 mm).
The supraspinatus was an ineffective depressor (average: 2.0 f 1.4 mm), as its line of action is almost
perpendicular to the glenoid, and its cross-sectional area
is of medium size. It caused a significantly ( P < 0.05)
smaller depression than that of the subscapularis and
the infraspinatus.
Depending on the glenohumeral abduction angle, the
pectoralis major either partially reversed or exacerbated
the humeral head superior translation as its line of action moved from inferior to superior with respect to the
glenoid. Depression of the humeral head in the hanging
arm position ( 3 . 4 f 0 . 7 mm) and 30" of glenohumeral
abduction (2.6 f 2.2 mm) changed to superior humeral
head translation in 60" of glenohumeral abduction
(-0.5 f 0.9 mm) and 90" of gelnohumeral abduction
(-0.7 f 0.5 mm).
Discussion
In preliminary experiments we were unable to identify
static constraints that would stabilize the glenohumeral
joint in the superior direction in the mid-range of motion. However, in the extremes of rotation, adduction
and abduction, the glenohumeral and coracohumeral
ligaments locked the humeral head in the center of the
glenoid. As the pathomechanism of superior decentralization of the humeral head is still unknown, the
210
A . M . Huldrr et a/. I Journul of Orthopardie Rrsrurch 19 (20011 206-212
purpose of this study was to investigate the contribution
of different muscles to superior stability of the gleno h umeral joint .
The latissimus and the teres major were most capable
of reversing superior translations of the humeral head.
Traditionally, the latissimus is described as a mover of
the shoulder joint causing adduction, extension, and
internal rotation [I 51 without any apparent stabilizing
function. However, the extent to which the latissimus is
necessary for shoulder function is unclear, as some investigators reported permanent deterioration of shouldcr function following surgical removal of the latissimus
[S] while some found only minor changes [2].
The rotator cuff muscles surrounding the glenohumeral joint act through force couples and serve as its
primary stabilizers. The horizontal plane force couple
consists of the subscapularis anteriorly and the infraspinatus posteriorly [3]. In the frontal plane, the deltoid
has the largest elevator moment arm that needs to be
counterbalanced inferiorly. The inferior rotator cuff
muscles have substantially smaller depressor moment
arms and may not be sufficient to counterbalance maximum deltoid activity. The latissimus dorsi, the teres
major and the pectoralis major have depressor moment
arms of the same dimension as the deltoid [19]. Consequently, these muscles may contribute to the inferior
part of the frontal plane force couple. Electromyographic studies that have documented activity in the
latissimus during abduction movements lend support to
this idea [18].
These findings suggest the usefulness of strengthening
and coordination excercises for the latissimus and the
teres major in the treatment of rotator cuff disease. They
also suggest avoiding surgical removal of the latissimus
dorsi. Whereas the humeral head depressing function of
the latissimus dimnished at higher degrees of abduction,
thc teres major had a constant effect due to its scapular
origin. The pectoralis major was the most variable
causing depression of the humeral head initially and
then elevation as the humerus was abducted. Although
the pectoralis major affected translations in vitro, an in
vivo stabilizing function is improbable according to
electromyographic studies [ 181. Further studies should
elucidate its in vivo function.
In our study, the infraspinatus and the subscapularis
showed similar depressor effects, although the effects
were smaller than the latissimus and the teres major. We
confirmed the findings of earlier cadaver experiments
that found that the whole rotator cuff [31], specifically
the infraspinatus, teres minor, and subscapularis muscles provide dynamic superior stability [5,27,3 11. Furthermore, we tested the superior and inferior portions of
the subscapularis separately because of their separate
innervation [17]. We found the inferior part to be a more
effective depressor because of its more inferiorly directed
line of action. NovC-Josserand identified the infraspin-
atus as a major active depressor of the humeral head
[24], and it seems important to surgically repair it
whenever possible to restore the horizontal and frontal
plane force couples.
Traditionally, the supraspinatus has been considered
to be important for superior stability and a complete
closure of rotator cuff defects involving the supraspinatus has been advocated [33].Indeed, the supraspinatus
is an important mover of the glenohumeral joint especially since it participates in the initiation of abduction
[10,34] and in rotation of the joint [12]. Although some
investigators reported a stabilizing effect in the anterior
and inferior directions [33], others found little contribution of the supraspinatus to superior stability [31,341.
Our study showed that the supraspinatus had a minor
superior stabilizing effect.
It is assumed that the long head of biceps tendon acts
as a primary depressor of the humeral head [37].In our
study it showed a considerable depression effect despite
its medium cross-sectional area. However, the long head
of biceps is minimally activated in shoulder movements,
indicating that it primarily serves as an elbow mover
[40]. It appears that the long head of the biceps tendon is
primarily a passive superior stabilizer in the glenohumeral joint [24,26].
The limitations of our study relate to the use of cadaveric specimens. We strived for the highest accuracy
possible using computer-controlled pneumatic actuators
and low-friction pulleys for muscle loading. Nevertheless, loading was based on the assumption that maximum muscle force is proportional to its cross-sectional
area (which was derived from the literature [36]). In each
position, the muscle loading was done sequentially and
at a force proportional to the cross-sectional area of the
muscle. This method neglected muscle interactions and
dependence of muscle activity on joint position. However, the study was designed to show potential effects of
single muscles in certain joint positions and not to replicate the exact in vivo situation precisely. Further in
vivo studies should elucidate their role.
Strings, representing lines of muscle action, were
adjusted according to the centroids of the tested muscles
(as derived from the literature). Changing lines of
muscle action accordingly simulated scapular inclination
relevant for thoracohumeral muscles. Although strings
are merely an approximation of the vaired lines of action of a muscle, they are a legitimate biomechanical
model of muscle forces. In our model, the effect of
negative intraarticular pressure was excluded as the joint
capsules were vented. This permits simulation of the
clinical situation in which a tear of the rotator cuff
prevents negative intraarticular pressure. The applied
constant forces d o not occur naturally but represent the
shear force component generated by muscles or gravity.
The clinical effect of contraction of any given muscle
might also differ from the effect demonstrated by
A.M. Halder et al. I Journul
of
Orthopaedic Research 19 (20011 ,706-212
isolated contraction of the muscle. Finally, we only
looked at whether an individual muscle could reverse the
superior translation. In vivo, their importance to glenohumeral stability would also be derived from their
contributions to concavity-compression at the joint.
These contributions would stabilize the glenohumeral
joint in all directions, including the superior direction
pol.
Acknowledgements
The first author was supported by the Max-Biederman-Institut, Berlin, Germany. The authors wish to
acknowledge F. Schulz, L. Berglund, and L. Berge from
the Orthopedic Biomechanics Laboratory and D. Larson from the Section of Biostatistics.
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