The glenohumeral joint is characterized by its mobility and
large range of motion. Various mechanisms are responsible for maintaining
glenohumeral stability2-4,8,12,13,15-18,20-23.
Although most of these mechanisms could potentially operate throughout
the entire range of motion, the relative importance of each depends
on whether the shoulder is in the mid-range or the end-range of
motion. The end-range is characterized by increased tensile force
on the static restraints of the capsule and its ligaments. All glenohumeral
motions that occur without increasing the capsular tension above
the baseline level are functionally in the mid-range19.
The glenohumeral ligaments serve as static stabilizers, preventing
excessive translation of the humeral head, particularly in the end-range
of motion3. Since the glenohumeral
joint is not stabilized by isometric articular ligaments, stability
in the mid-range must be achieved by mechanisms other than capsuloligamentous
restraints. Many authors have noted that muscle activity across
a joint leads to increased stability2,4,8,13,15-18,20-22.
Concavity compression is a stabilizing mechanism by which muscular
compression of the humeral head into the glenoid fossa stabilizes
the glenohumeral joint against shear forces13,15,16.
The resulting stability is related to the depth of the concavity
and the magnitude of the compressive force. Matsen et al.15,16 proposed use of the stability
ratio (the translation force at dislocation divided by the compressive load)
to compare the effectiveness of concavity compression under different
conditions. Concavity compression is probably the most important
stabilizing mechanism in the mid-range of motion. It has been assumed,
but not proved, that concavity compression is important in the end-range
of motion as well. However, it is unknown whether the glenohumeral
ligaments or muscles provide greater restraint in the end-range
of motion12. The relative importance
of these factors may vary according to the position of the glenohumeral joint.
The purpose of the current study was twofold. First, we sought
to define a new biomechanical parameter that would better reflect
the contribution of muscle forces to joint constraint. To that end, we
measured the actual compressive and shear force components generated
by each rotator cuff muscle. Combining the force components with
the concavity-compression mechanism, we were able to calculate what
we termed the dynamic stability index. This parameter reflects not
only the concavity-compression mechanism but also the line of action
of each muscle force. Second, we sought to compare the dynamic stability
provided by the rotator cuff muscles in the mid-range and end-range of
motion, particularly in the position of anterior shoulder instability,
with use of the dynamic stability index.
Preparation of Specimens
Ten fresh-frozen shoulders (six right and four left shoulders)
were obtained from human cadavera and were kept frozen at -20 degrees
Celsius. The ages of the subjects had ranged from forty-eight to
seventy-four years at the time of death. The specimens were thawed
at room temperature for twenty-four hours before dissection. All
soft tissues, except for the tendons and muscles of the rotator
cuff (the subscapularis, supraspinatus, infraspinatus, and teres
minor) were removed. The glenohumeral joint was disarticulated after
the rotator cuff muscles were released from the scapular origin.
The glenohumeral capsule was resected along with the coracohumeral
and glenohumeral ligaments, while the glenoid labrum was preserved.
The neck of the glenoid was osteotomized 2.5 centimeters medial
to the articular surface.
Testing Apparatus
A specially designed Plexiglas frame was constructed to permit
placement of the humerus in the desired positions of abduction-adduction,
flexion-extension, and internal-external rotation with respect to
the scapula (Fig. 1).
The distal aspect of the humeral shaft was firmly fixed in a 7.7-centimeter-diameter
epoxy-putty cylinder. The cylinder was fixed to the rotating joint
of the frame, on which a load-cell (AMTI model FS 160A-600; Barry
Wright, Watertown, Massachusetts) was mounted. The humerus-rotating
joint-load cell unit was attached to the fixation frame, while the
approximate center of rotation of the humeral head was placed in
the center of the frame with the aid of a laser-pointing device.
In humans, the scapula is anteriorly protracted by 30 degrees with
reference to the coronal plane18.
The so-called anatomical neutral position is the position in which
the humerus hangs at the side (parallel to the medial border of
the scapula) in 0 degrees of rotation (that is, when the elbow is flexed,
the forearm is perpendicular to the coronal plane).
The osteotomized glenoid was reattached to the neck of the scapula
with two Kirschner wires. The scapula was rigidly fixed to a specially
designed mounting device that permitted the excursion of lines that
were connected to each rotator cuff muscle around the scapula. The
mounting device enabled the scapula and its glenoid to be anatomically
aligned in relation to the humeral head in any desired position
of the glenohumeral joint. Before data collection, the Kirschner
wires were removed from the scapula and the glenoid was removed
in order to avoid bone contact between the humerus and the scapula,
which could have affected the measurement of the force components
(Fig. 2).
After the glenoid was removed, the position of the humeral head
was maintained by secure fixation of the whole frame, including
the humerus-rotating joint-load cell unit.
A single line of action following the centroid of each muscle,
which was determined with magnetic resonance imaging, was used for
the simulated muscle contractions. The tendon-muscle clamp-cable
systems were routed through a system of pulleys around the scapula.
A constant force of twenty newtons was applied to each muscle by means
of a hanging-weight system.
A six-degrees-of-freedom electromagnetic tracking device (Fastrak;
Polhemus Navigational Sciences Division, Colchester, Vermont) was
used to measure the position and orientation of the humerus at the
glenohumeral joint. The source was secured to the table of the testing
frame, and the sensor was secured to the humeral side of the rotating-hinge
joint. The load-cell permitted accurate resolution of the forces
that were applied to the humeral head by the rotator cuff muscles.
Definition of Anatomical Axes
We defined flexion and extension as forward and backward rotation
of the humerus about a horizontal axis perpendicular to the face
of the glenoid; abduction, as outward rotation about a horizontal
axis parallel to the face of the glenoid; and external and internal
rotation, as outward and inward rotation of the humeral shaft. The
anatomical axes used for the measurement of force components were
defined as being in line with the anterior-posterior and superior-inferior
axes of the glenoid. The medial-lateral axis was defined as being
perpendicular to both of these axes.
Data Acquisition and Analysis
Testing was performed with the glenohumeral joint in 60 degrees
of abduction, 45 degrees of extension, and five positions of external
rotation (achieved by rotating the humerus from neutral rotation
to 90 degrees of external rotation in intervals of 22.5 degrees).
The position of the glenohumeral joint in 60 degrees of abduction
corresponded with the position of a normal shoulder joint in 90
degrees of abduction. The force components that were generated by
each rotator cuff muscle-tendon unit in the medial-lateral (compression),
anterior-posterior (shear), and superior-inferior (shear) directions
were measured at each glenohumeral position before and after the
application of the constant twenty-newton force to each muscle.
The data that was obtained before force application was used as
a reference (the zero-load condition). Raw load-cell data was then
transformed three-dimensionally, according to the defined anatomical axes,
on the basis of the position data derived from the spatial sensor.
To verify the accuracy of the measurements, a vector summation of
the three measured force components for each muscle was compared
with the applied force in each glenohumeral position, and calculations
were performed as follows:
where Fcomp, FA-P shear, and FS-I shear denote the measured compressive,
anterior-posterior shear, and superior-inferior shear components,
respectively. The denominator of these equations represents a vector
sum of the measured force components.
A new biomechanical parameter, the dynamic stability index, was
used to represent the combined stabilizing effects of the rotator
cuff muscle force components and the concavity-compression mechanism
of the glenohumeral joint. The dynamic stability index of a rotator
cuff muscle in the anterior direction is the maximum anterior dislocating
shear force imposed on the humeral head that can be stabilized by
two forces that result from muscle activity. The first force is
the shear load that can be resisted by the reaction of the compressive
force component of the muscle through the concavity-compression
mechanism. The second force is the shear force component of the
muscle in the anterior-posterior direction that can decrease or
increase the stability in the anterior direction. In order to calculate
the first force, we employed the concept of the stability ratio16-18, a dimensionless variable describing
the maximum dislocating force in a given direction that can be stabilized
by the compressive muscle load on the glenoid fossa (concavity-compression),
assuming that frictional effect is minimal. A stability ratio of
0.35 was used for the anterior direction. This value is consistent
with published data regarding the concavity-compression mechanism for
the glenohumeral joint with the labrum intact16,17.
The stability ratio may vary according to labral height, cartilaginous
depth, compliance of tissues, and friction16.
The dynamic stability index is expressed as the percent ratio of
the dislocating shear force to the rotator cuff muscle force. The
dynamic stability index in the anterior direction can be calculated
as: dynamic stability index = (percent compressive force ¥ stability
ratio in anterior direction) - percent anterior shear force.
For example, if the infraspinatus contracts to generate a fifty-newton
force, if the percent compressive and anterior shear force 852components of
the muscle are 90 and 20 percent, respectively, and if the stability
ratio of the glenoid in the anterior direction is 0.35, then the
maximum anterior dislocating shear force that could be stabilized
by the compressive force component of the infraspinatus through
the concavity-compression mechanism would be: 50 newtons ¥ 0.9 ¥
0.35 = 15.75 newtons. The anterior shear force component generated
by the infraspinatus would be: 50 newtons ¥ 0.2 = 10 newtons. The
anterior-posterior shear force generated by the muscle itself would destabilize
or stabilize the joint independent of the glenoid geometry. Thus,
the final maximum anterior dislocating shear force that could be
stabilized by the compressive (concavity-compression) and anterior
shear force components generated by muscle contraction would be:
15.75 newtons - 10 newtons = 5.75 newtons. Since the dynamic stability
index is the percent ratio of the maximum anterior dislocating shear
force to the rotator cuff muscle force, the dynamic stability index
of the infraspinatus in the anterior direction would be: 5.75 newtons/50
newtons x 100 percent = 11.5 percent. Thus, the higher the dynamic
stability index of a rotator cuff muscle in the anterior direction,
the greater the dynamic glenohumeral stability provided by the muscle.
All of the percent force components, and the dynamic stability
index with the humerus in neutral and in 90 degrees of external
rotation, were compared, with use of analysis of variance (two-way
layout with equal numbers of observations in the cells), to determine
the force range for all specimens.
Rotator Cuff Muscle Force Vectors
The line of action of each rotator cuff muscle-tendon unit, representing
the direction of its force vector, was grossly observed by noting
the relative positions of the origins, insertions, and centroids of
each muscle belly. With the humerus in neutral rotation, representing
the mid-range of glenohumeral motion, all of the muscles appeared
to have compressive and inferior shear force components. The subscapularis
and supraspinatus appeared to generate posterior shear force components
in addition to compressive force components. The infraspinatus and
teres minor forces showed lines of action that could be resolved
into compressive and anterior shear force components (Fig. 3).
With the humerus in 90 degrees of external rotation, 60 degrees
of abduction, and 45 degrees of extension, representing the position
of anterior shoulder instability, the supraspinatus and infraspinatus
produced both superior shear and compressive force components. The
shear force components generated by the subscapularis and teres
minor did not appear to change in the superior-inferior direction.
The line of action of the supraspinatus demonstrated a large anterior
shear force component. The subscapularis demonstrated an anterior
shear force component, whereas the infraspinatus and teres minor
generated posterior shear force components (Fig. 4).
Compressive Force Components
The magnitude of the compressive force component generated by
each rotator cuff muscle changed substantially as the humerus was
rotated from neutral (the mid-range of motion) to 90 degrees of
external rotation (the end-range of motion) (Fig. 5-A). The rotator
cuff muscles were primarily compressors in both the mid-range and
the end-range of motion in that the magnitudes of the compressive
force components were more than 85 percent of each simulated muscle
force in these ranges.
With the humerus in neutral rotation, the magnitudes of the compressive
force components averaged 90, 85, 98, and 96 percent of the forces applied
to the teres minor, infraspinatus, supraspinatus, and subscapularis
muscles, respectively (Table I). The supraspinatus and subscapularis
generated significantly larger compressive components than did the
teres minor and the infraspinatus (p < 0.05). A reversal of
this pattern was noted with the humerus in 90 degrees of external
rotation, simulating the position of anterior shoulder instability. The
magnitudes of the compressive force components generated by the
teres minor and infraspinatus increased significantly, to 99 and
96 percent, respectively (p < 0.05). Conversely, the magnitudes
of the compressive force components generated by the supraspinatus
and subscapularis decreased significantly, to 86 and 93 percent,
respectively (p < 0.05). The compressive force components generated
by the supraspinatus in this position were significantly lower than
those generated by the infraspinatus (p < 0.05) and the teres minor
(p < 0.001) (Table I).
Anterior-Posterior Shear
Force Components
The anterior-posterior shear force components generated by each
rotator cuff muscle changed significantly with rotation of the humerus (p < 0.05).
This finding confirmed the observations made by studying the lines
of action according to each muscle-tendon origin, insertion, and centroid
(Fig. 5-B).
With the humerus in neutral rotation, the teres minor and infraspinatus
generated anterior shear force components averaging 19 and 16 percent
of the applied forces, respectively, whereas the supraspinatus and
subscapularis generated posterior shear force components averaging
12 and 26 percent of the applied forces, respectively. As the humerus
was externally rotated to 90 degrees, the directions of the shear
force components generated by these four muscles reversed compared
with those generated in the neutral position (Table I). The teres
minor and infraspinatus generated posterior shear force components
averaging 2 and 8 percent of the applied forces, respectively; these values
were significantly different from those generated in the neutral
position (p < 0.05). The supraspinatus, on the other hand, generated
a destabilizing anterior shear force component averaging 31 percent
of the applied force; this value was significantly different from
that generated in the neutral position (p < 0.05). The subscapularis also
generated an anterior shear force component that represented a significant
change from the force generated in the neutral position (p < 0.005).
Superior-Inferior Shear
Force Components
As with the anterior-posterior shear force components, the magnitude
of the superior-inferior shear force components varied significantly with
humeral rotation (p < 0.05) (Table I). With the humerus in neutral rotation,
the shear force components generated by all four muscles were directed
inferiorly; as the humerus was rotated externally more than 67.5
degrees, however, the shear force components generated by the infraspinatus
and supraspinatus were directed superiorly (Fig. 5-C).
Dynamic Stability Index
in the Anterior Direction
The dynamic stability index in the anterior direction, calculated
with use of 0.35 as the stability ratio, was significantly different
for all four muscles when the humerus was in neutral rotation (the mid-range
of motion) compared with 90 degrees of external rotation (the end-range
of motion) (p < 0.05) (Table II).
In the mid-range of motion, the dynamic stability indices for
the supraspinatus and subscapularis were greater than those for
the infraspinatus and teres minor (p < 0.05). As the humerus
was externally rotated to 90 degrees, the dynamic stability indices
for the teres minor and infraspinatus increased significantly (p < 0.05)
whereas those for the supraspinatus and subscapularis decreased significantly
(p < 0.05). In the end-range of motion, with simulation of the
position of anterior shoulder instability, the subscapularis, infraspinatus,
and teres minor had significantly greater dynamic stability indices
than did the supraspinatus (p < 0.005). The supraspinatus had
the lowest dynamic stability index in the end-range of motion because
it generated the highest anterior shear force component as well
as the lowest compressive force component in that position.
The glenohumeral joint is a unique articulation that, under normal
circumstances, maintains a balance between its high degree of mobility
and its lack of intrinsic stability. Both static and dynamic factors
are responsible for glenohumeral stability2-4,8,12,13,15-18,20,23.
The glenohumeral ligaments, which prevent excessive translation
of the humeral head in the end-range of motion, remain tension-free
until glenohumeral motion approaches its terminal range19. In the mid-range of motion, during
which there is no increase in capsular tension, dynamic glenohumeral
stability must be provided by active muscle contraction. A number
of studies have suggested that the glenohumeral capsule and ligaments
work in combination with the dynamic stabilizing effects of the
rotator cuff muscles2,5,21. Although
these stability mechanisms could potentially operate throughout
the entire range of motion, the relative importance of static and
dynamic factors may vary according to the position of the glenohumeral
joint.
All muscle forces spanning the shoulder joint can be resolved
into compressive and shear components. The compressive force component
stabilizes the glenohumeral joint by the mechanism referred to as
concavity-compression13,15,16.
The resulting stability is related to the depth of the concavity
and the magnitude of the compressive force15.
In the present study, the compressive force vectors generated by
the individual rotator cuff muscles changed substantially as the
humerus was rotated from neutral rotation to full external rotation.
The rotator cuff muscles were confirmed to be primarily compressors,
as the compressive components were far greater than the shear components
regardless of humeral rotation. However, the shear force component
generated by each rotator cuff muscle directly affects the stability
in a given direction. The present study showed that shear force
could either stabilize or destabilize the joint, depending on its
direction. It is notable that the infraspinatus and teres minor
generated posterior shear forces and increased compressive forces in
the end-range of motion, thereby enhancing the stability of the
joint. Conversely, the supraspinatus generated a large anterior
shear force in the end-range of motion, thereby destabilizing the
joint in the anterior direction. Since the capsule and ligaments
were transected in the present study, our model took into consideration
muscle action in the absence of static restraint. In the end-range
of motion, muscles have the potential for generating increased compressive
force by tensioning the capsule (like a nutcracker) on the opposite
side of the joint.
We used a new parameter, the dynamic stability index, to more
realistically represent the biomechanical role of the force vectors
providing dynamic glenohumeral stability. The dynamic stability
index of a muscle reflects both the concavity-compression mechanism
and the shear force generated by the muscle itself. In the mid-range
of motion, the dynamic stability index (calculated with use of a
stability ratio of 0.35) demonstrated that the subscapularis and
supraspinatus provided significantly greater dynamic stability in
the anterior direction than did the posterior cuff muscles (p < 0.05).
Conversely, in the end-range of motion, the dynamic stability index
revealed that the subscapularis, infraspinatus, and teres minor
provided significantly greater stability than did the supraspinatus
(p < 0.005). Notably, the supraspinatus provided the least dynamic
stability in the end-range because it generated the highest anterior shear
force as well as the lowest compressive force in that range.
The dynamic stability index defined in this study facilitates
comparison of the stabilizing and destabilizing roles of the rotator
cuff muscles and also serves as a reference for interpreting the
results of other shoulder stability studies related to the action
of any of the rotator cuff muscles. Cain et al.4 found
that the infraspinatus and teres minor play an important role in
the anterior stability of the shoulder. Jobe et al.10 noted that the posterior rotator
cuff muscles are quite active during late cocking, when the shoulder reaches
a position of approximately 90 degrees of abduction, 30 degrees
of horizontal extension, and 90 to 120 degrees of external rotation.
The present study demonstrated quantitatively that the posterior
rotator cuff muscles reduce strain on the anterior structures of
the glenohumeral joint by pulling the humeral head posteriorly and
by increasing the compressive force during external rotation of
the shoulder.
The maximum muscle force may be estimated on the basis of the
physiological cross-sectional area of each muscle1,9.
In the current study, the total compressive force generated by the
four rotator cuff muscles in the end-range of motion was not significantly
different from that in the mid-range when the compressive force
components of each muscle were normalized by the proportional physiological cross-sectional
area of each muscle (p > 0.05)1,11,17.
When the dynamic stability index was normalized in the same way,
the total dynamic stability provided by the four rotator cuff muscles
in the end-range of motion was approximately 20 percent less than
that in the mid-range. This difference can be attributed to a decrease
in the dynamic stability index for the subscapularis in the end-range,
as this muscle has the largest proportional physiological cross-sectional
area.
Individual muscle activity during function can be estimated directly
on the basis of electromyographic signals14.
Gowan et al.6 analyzed electromyographic
signals in baseball players during pitching and reported that, during late
cocking, as the shoulder reached extreme external rotation, the
subscapularis had the most activity, followed by the infraspinatus
and the teres minor; the supraspinatus had the least activity. The present
study revealed that, in the end-range of motion, the dynamic stability
index in the anterior direction was significantly greater for the
subscapularis, infraspinatus, and teres minor than it was for the
supraspinatus. Therefore, dynamic glenohumeral stability in the
end-range of motion may be comparable with that in the mid-range
when it is taken into consideration that the subscapularis, with
the largest physiological cross-sectional area, had increased electromyographic
activity while the supraspinatus, which provided the least effective
dynamic stability, had decreased activity in the end-range.
Glousman et al.5 reported that
patients who had chronic anterior instability of the shoulder had
markedly lower electromyographic activity in the infraspinatus and subscapularis
during late cocking. The levels of activity in the supraspinatus
increased throughout the cocking phase. Those authors, on the basis
of our results, would have been able to directly relate the patterns
of altered electromyographic activity to the factors that contributed
to the instability. Clinically, this suggests that the rehabilitation
of rotator cuff muscles in patients with anterior shoulder instability
should be directed differently than otherwise would have been thought,
with emphasis on the internal and external rotators.
The current study had several limitations. First, simulated muscle
contractions based on a single line of action might be different
from muscle contraction in vivo. However, we reproduced
the line of action that was determined previously in anatomical
and magnetic resonance imaging studies of the shoulder4. Second, muscle length-tension relationships7 differ according to shoulder position
(that is, the length of the muscle). To account for this variable, the
force components and the dynamic stability indices in this study
were defined as percentages of the force applied to each muscle.
Third, there is some controversy regarding the scapulohumeral position
that best simulates anterior shoulder instability. The normal scapula
is anteriorly rotated approximately 30 degrees with respect to the
coronal plane18. In the cocking
position, the humerus moves posteriorly in the coronal plane, altering
the scapulohumeral relationship. Our model approximated the extreme
motion in the late-cocking phase of pitching.
In summary, we showed that the dynamic glenohumeral stability
provided by each of the rotator cuff muscles can be quantified with
use of the dynamic stability index defined in this study. The dynamic
glenohumeral stability provided by the rotator cuff muscles was
important in the end-range of motion as well as in the mid-range.
A glenohumeral joint with a lax capsule might be stabilized dynamically
in the vulnerable end-range of glenohumeral motion if the glenoid
concavity is maintained and if the function of the external and internal
rotators, which are efficient stabilizers in this position, is enhanced.