Contribution of the passive properties of the rotator cuff

to glenohumeral stability during anterior-posterior

loading

Richard E. Debski, PhD, Masataka Sakane, MD, Savio L.-Y. Woo, PhD, Eric K. Wong, BS,
Freddie H. Fu, MD, and Jon J. P. Warner, MD, Pittsburgh, Pa

The passive properties of the rotator cuff have been shown result of the thin posterior joint capsule compared with the
to provide some stabiliv during anterior-posterior (AP) anterior capsule, which has several thickenings. This infor-
trans/ation. However, the relative importance of the rotator mation increases our understanding of posterior stabili~ at
cuff to joint stability remains unclear. The purpose of this the glenohumeral joint during clinical laxiv tests. 0 Shoul-
study was to quart@ the force contributions of the rotator der Elbow Surg I999;8:324-9.)
cuff and of capsuloligamentous structures at the gleno-
humeral joint during AP loading. We hypothesized that the GI eno h umeral joint stability is provided by a complex
rotator cuff acts as a significant passive stabilizer of the combination of both static and dynamic factors, includ-
glenohumeral joint and that its contribution to joint stability ing the rotator cuff and capsuloligamentous structures.
is comparable to the contribution made by the components The main contribution of the rotator cuff muscles to joint
of the glenohumeral capsule. A robotic/universal force- stability is the ability to increase joint compression,
moment sensor testing system was used to determine both thereby maintaining the humeral head within the gle
the multiple “degrees of freedom” joint motion and the in noid cavity. This has been termed concavity compres-
sion by Lippitt et al. 15 Most research has therefore
situ force carried by each soft tissue structure during appli-
focused on the active role of the rotator cuff in provid-
cation of an 89N AP load at 4 abduction
The percent contribution of the rotator
angles.
cuff to the resisting
ing joint stability.2-4,8,16.17,26,35
Nevertheless, the rotator cuff does contribute to
force of the intact joint during AP loading was significantly anterior-posterior (AP) joint stability through its pas-
greater during posterior loading (35% -+ 26%) than during sive properties or bulk effect.13 A number of
anterior loading at 60” of abduction (P < .05). The contri- authors’4,21,22,24,32 have sought to demonstrate this
bution of the rotator cuff (ie, 29% * 16% at 30” of abduc- effect by applying a constant load to the joint and
tion] was Found to be significantly greater than the contri- measuring the change in translation of the humeral
butions of the capsule components during posterior loading head that results from removal of a specific structure.
at 309 604 and 90” of abduction (P < .05). However, no Presently, the amount of in situ force carried by the
differences could be found bebeen the respective contribu- rotator cuff and the capsuloligamentous components
tions of the rotator cuff and the capsule components during as well as the relative importance of the rotator cuff
to joint stability during AP loading remain unclear.
anterior loading. The results support our hypothesis and
Such information is particularly useful when consider-
suggest that passive tension in the rotator cuff plays a more
ing the relative importance of the capsular structures
significant role than other soft tissue structures in resisting in providing joint stability during clinical examina-
posterior loads at the glenohumeral joint: The important tions and capsular shift procedures.
role of the rotator cuff during posterior loading may be a The purpose of this study was to quantify the force
contributions of the rotator cuff and capsuloligamentous
From the Musculoskeletal Research Center, Department of structures at the glenohumeral joint to joint stability dur-
Orthopaedic Surgery, University of Pittsburgh. ing AP loading in a cadaveric model. We hypothe-
Su ported by the Whitaker Foundation and the University of Pitts- sized that the rotator cuff acts as a significant passive
g urgh Medical Center. stabilizer of the glenohumeral joint and that its contri-
Reprint requests: Richard E. Debski, PhD, Musculoskeletal bution to joint stability is comparable to the contribution
Research Center, Department of Orthopaedic Surgery, Univer-
of the components of the glenohumeral capsule. We
sity of Pittsburgh, 210 Lothrop St, PO Box 71 199, Pittsburgh,
PA 15213. used a robotic/universal force-moment sensor testing
Copyright 0 1999 by Journal of Shoulder and Elbow Surgery system to determine the in situ forces of the various
Board of Trustees. structures crossing the joint during glenohumeral
1058-2746/99/$8.00 + 0 32/l/94927 motion without contacting the soft tissue.lOJ5

324
J Shoulder Elbow Surg
Volume 8, Number 4
MATERIALS AND METHODS
Experimental Apparatus
A robotic manipulator and a universal force-moment sen-
sor (UFS) (Figure 1) were utilized to examine the function of
the soft tissue structures at the glenohumeral joint. This
robotic/UFS testing system can direct1 measure in a non
contact manner the in situ force of a so I tissue structure dur-
ing application of external loads to the joint or during a pre
scribed motion. The robotic manipulator can also determine
the motion of a joint in response to specified external loads.
By using positioncontrol mode, the robotic manipulator can
reproduce the joint motion at any time, including after the
specimen has been altered (for example, after removal of a
ligament). Thus the principle of superposition can be
applied, and the magnitude and direction of the in situ
force of the removed structure can be determined.
The robot is a 6-axis, serial-articulated manipulator (Uni-
mate, Puma Model 762) with a repeatability of 0.02 mm
for position and 0.02” for orientation.25 force-moment
data collection is achieved with a UFS (JR Model 4015,x
Woodland, Calif) that provides force-moment feedback
during determination of the kinematic response of the joint
to an external load and forcemoment data during position
control. Repeatability of the sensor is better than 0.2 N for
forces and 0.01 Nm for moments.
The princi le of superposition, as a plied to the exper-
iments descri E ed in this study, allows tRe determination
magnitude and direction of the in situ forces in soft tissue
structures at the glenohumeral joint. The requirements to
ensure the validity of this principle are: (I) no interaction
between elements; (2) the bony tissue is rigid relative to the
Ii aments; and (3) the positions of the bones are re eat-
a% le. Because of interaction among the skin and de Ptoid,
rotator cuff, and glenohumeral joint ca sule, the resultant
forces are a close approximation of tRe actual force in
each structure. As for the joint capsule, the interaction
between each individual component was quantified by
examining the difference in forces before and after sepa-
ration of each component.6
Experimental Methodology
Ten fresh cadaveric shoulders were wrapped in saline-
soaked gauze and stored in plastic bags at -20” C until dis-
section. Before the day of the test, each specimen was
thawed overnight at room temperature. Each shoulder was
then dissected free of all skin and musculature below the
deltoid tuberosity on the humerus and the inferior half of
the scapula. The joint was also vented to atmospheric pres-
sure through a small incision in the rotator interval, elimi-
nating the effect of this parameter from all testing proce-
dures. Before removal of the humeral condyles, their ali n-
ment with respect to the humeral shaft was recorded % y
placing a Kirschner wire throu h the humeral shaft parallel
to the axis formed by the con 8 les. The humerus was then
potted in epoxy putty, secure cy within a thick-walled alu-
minum cylinder, and fixed in a custom clamp mounted to
the base of the robotic manipulator. The scapula was fixed
in a block of epoxy pu and rigidly attached to the end
effector of the mani “ru ator through another specially
designed clamp and t Re UFS.
Standard reference positions were obtained at 4 abduc-
tion angles for each external loading test. The joint was ini-
Debski et al 325
of robotic/UFS testing system with
Soft tissue structures are not shown
humerus and scapula in the clamps.
tially positioned in the test system at 0” forward
flexion/extension and 0” abduction in the scapular plane;
anatomic humeral rotation was determined by having the
of humeral condyles rotated posteriorly approximately 30
from the scapular plane. Force control was then used to
apply a 22-N compressive force (medially directed) to the
humerus while the forces in the 2 orthogonal directions
were minimized (approximately 0 N). Such application of
force served to center the humeral head within the lenoid
cavity and determined the joint position at 0” of ab J uction.
The abduction angle was then increased by 30” and
force control again was used to position the humeral head
within the glenoid while maintaining a 22-N compressive
load and minimizing the forces in the other directions. This
iterative scheme was used for the entire range of gleno-
humeral abduction so that reference positions were
obtained at o”, 30”, 60”, and 90” of abduction. Forward
flexion/extension and internal/external rotation of the
humerus were fixed while the control system “learned” and
then recorded the position of the joint at each abduction
angle. AP radio raphs were taken at each abduction posi-
tion to confirm ta at the humeral head was centered within
the glenoid cavity. Improper positioning of the humeral head
within the glenoid cavity was an indication of ‘oint patholo-
gy, and such specimens were not included in tll e study.
AP loading tests involved a maximum of 89 N ap lied to
the scapula in the anterior and posterior directions. TRe start-
ing position for all tests was defined by the previously
obtained abduction positions (humeral head centered in gle-
noid cavity). Initially the control system attempted to meet 2
force targets at 0” of abduction: 22-N ‘oint compression and
10% increments of the maximum loa cl of 89 N (ie, 8.9 N,
17.8 N, and so forth). The scapula could translate along
each of the 3 axes to meet the required force targets while
the rotational degrees of freedom (abduction, forward flex-
ion/extension, and internal/external rotation) were held
constant. This experiment therefore constitutes a “3 degrees
of freedom” loading test. Preconditioning was then per-
formed by cycling the specimens through the joint positions
326 Debski et al J Shoulder Elbow Surg
July/August 1999

0 Anterlor
I n Posterior
q Anterior
I Posterlor

0 30 60 90 0” 30” 60” 90”

Abduction (“)
Abduction (“)
Figure 2 AP translation (mean * SD) of intact glenohumeral joint
caused by application of AP load of 89 N. Figure 3 In situ force (mean * SD) in rotator cuff caused by appli-
cation of 89-N load.

found for anterior and posterior loading 10 times. The AP percent contribution to the force-resisting joint motion. The
loading protocol was subsequently repeated to determine effect of abduction an le on the magnitude of the translation
the final joint positions for each loading condition. The joint in the direction of loa 3 ing was examined with l-way analy-
was then abducted to the 30”, 60”, and 90” positions, and sis of variance (ANOVA). Significance was set at P c .05.
the AP loading and preconditioning rotocols were repeat- The effect of abduction angle and structure on the magni-
ed. The robotic manipulator recorde cr the AP, su erior-inferi- tude of the in situ force was examined with 2-way ANOVA.
or, and medial-lateral translations at the joint tRat resulted Finall , the percent contributions of each structure were com-
from application of the AP load while the UFS recorded the pare CTfor each abduction angle with 2-way ANOVA.
resultant forces and moments at each loadin position.
After determination of the ‘oint positions 7 or each exter- RESULTS
nal loadin condition with a II soft tissue structures intact, AP translation increased with increased AP load.
the in situ f orce in each structure was determined. This was Translations in both the anterior and posterior direc-
accomplished by using the robot in position control and tions (Figure 2) were smaller at the extremes of abduc-
having it step throu h the joint positions found for loadin tion (0’ and 907 than in the mid-range (30” and 60”)
of the intact joint be 3ore and after a structure was remove ? .
under maximum loading (P c .05). Joint motion was
The test system recorded these “new” forces and moments
at the joint after the structure was removed. Seven struc- restricted in some cases by contact between either the
tures were removed in the followin order: (1) skin and del- acromion (posteriorly) or coracoid (anteriorly) and the
toid musculature; (2) rotator cuf 9; (3) separation of the humerus at every abduction angle. Bony contact was
glenohumeral capsule regions; (4) superior glenohumeral confirmed visually and by noting residual forces and
and coracohumeral ligaments (SGHL/CHL); (5) middle moments after soft tissue removal. All glenohumeral
glenohumeral ligament (MGHL); (6) anterior band of the joints subluxed as a result of the application of the 89-
inferior glenohumeral ligament (AB-IGHL ; and (7) posteri- N load in both the anterior and posterior directions.
or band of the IGHL (PB-IGHL). The di I erence in forces The resultant forces at the joint were not found to
before and after each structure is removed determines the change significantly after repetition of the joint kine-
force in each structure at a given joint position.
matics resulting from initial application of the external
“Separation” of the glenohumeral capsule included per-
foration along the border of 7 specific regions but not load, which indicates that these large subluxations did
removal of any soft tissue. The 7 regions of the capsule not damage the capsule or other soft tissue structures.
were (1) SGHL/CHL, (2) rotator interval, (3) MGHL, (4) AB- The magnitude of the in situ force carried by the rota-
IGHL, (5) axillar pouch of IGHL, (6) PB-IGHL, and (7) os- tor cuff at the maximum load of 89 N in each direction
terior capsule. Tl is procedure allowed quantification o Pthe of loading are shown in Figure 3. The rotator cuff car-
interaction between the different portions of the capsule ried large forces during all experiments, and these
correspondin to the load transmitted transversely through- forces were found to change with direction of loading
out the capsu Be. and with the abduction angle. The magnitude of the in
The magnitude and direction of the in situ force in each
situ force reached a minimum at 30” of abduction and
of the 7 aforementioned structures was obtained at all joint
a maximum at 90” of abduction during anterior load-
ositions during AP loading. The component of the in situ
Porce of each structure in the direction of loading (either ing. During posterior loading, the in situ force was a
anterior or posterior) was also determined and normalized maximum at 60” of abduction and a minimum at 90”.
to the magnitude of the externally applied load. This quanti- Directional data indicated that the resultant force of the
ty was expressed as a percentage to obtain the structure’s rotator cuff always applied tensile forces to the scapula.
J Shoulder Elbow Surg Debski et al 327
Volume 8, Number 4

0 Anterior U Anterior
H Posterior .
bCO.051 n Posterior
W.05) 'ii‘ 60- I I I I
b * * * *
5 so-
'E
3 40-
n
g 30-

6 20-
E
$ lo-
f T T
n 0
Rotator Cuff SGHUCHL MGHL AB-IGHL PB-IGHL Rotator Cuft SGHUCHL MaHL AS-IGHL PB-IGHL
0” Abduction 60’ Abduction

Figure 4 Percent contribution [mean * SD) of rotator cuff and Figure 6 Percent contribution (mean * SD) of rotator cuff and
capsuloligamentous components to resisting force during applica- capsuloligamentous components to resisting force during applica-
tion of 89-N external load at 0” abduction. tion of 89-N external load at 60” abduction.

0 Anterior 0 Anterior
@4.05) WPosterior 9 60 @<o.OS> n Posterior
@ I I I I
5 50 * * * *

Rotator cuff SGHLKHL MGHL AB-IGHL PB-IGHL Rotator Cuft SGHLICHL MGHL AB-IGHL PB-IGHL
SO” Abduction
30’ Abduction

Figure 5 Percent contribution (mean * SD) of rotator cuff and Figure 7 Percent contribution (mean * SD) of rotator cuff and
capsuloligamentous components to resisting force during applica- capsuloligamentous components to resisting force during applica-
tion of 89-N external load at 30” abduction. tion of 89-N external load at 90” abduction.

DISCUSSION
The percent contribution of the rotator cuff to the
resisting force of the intact joint during AP loading In this study new experimental methods were used to
also varied with both the direction of applied loading quantify the force contribution of the soft tissue struc-
and the abduction angle (Figures 4 through 7). The tures to glenohumeral stability during AP loading of an
contribution of the rotator cuff was significantly intact joint. A robotic/UFS testing system was used to
greater during posterior loading (35% * 20%) than meosure the kinematic response of intact shoulders dur-
during anterior loading at 60” of abduction (7% * ing application of an external load to the joint and to
7%) (P < .05). The contribution of the rotator cuff determine the in situ force in the surrounding muscula-
(26% * 19% at 0” abduction, 29% * 16% at 30” ture and glenohumeral joint capsule. The resultant
abduction, and 19% f 13% at 90” abduction) was quantitative data might aid the diagnosis of and treat-
also found to be significantly greater than the contri- ment protocols for glenohumeral joint injuries.
butions of all the capsule components during posteri- The rotator cuff has been shown to contribute to joint
or loading at all abduction angles (P < .05), except stability through several mechanisms, including (1) com-
for the contribution of the SGHL/CHL at 0” of abduc- pression of the articular surfaces,15 (2) tightening the
tion (26% f 19%). No statistically significant differ- passive ligamentous constraints,’ (3) barrier effect of
ences could be shown between the respective contri- contracted muscle,27 and (4) bulk effect or passive mus-
butions of the rotator cuff and the capsule compo- cle tension.14Jl Several studies2lJsJ4 found the
nents during anterior loading (P > .05). supraspinatus and the infraspinatus/teres minor to be
328 Debski et al J Shoulder Elbow Surg
July/Augusf 1999

important posterior stabilizers of the glenohumeral joint. commonly described function of the glenohumeral joint
These studies measured the change in translation of the capsule. The soft tissue structures restrict motion more at
humerus with application of a constant load. In contrast, the extremes of motion (0“ and 90” of abduction) than
the glenohumeral joint was not predisposed to disloca- in the mid-range (30” and 60”). The kinematic response
tion when Warren et al34 excised the posterior rotator of the joint to the passive properties of the rotator cuff
cuff. Using the same technique, Turkel et ,132 found that and deltoid musculature determined by this study sup
the subscapularis tendon acted as a significant anterior ports the results of other studies9~1*~16~1*l*0,32,33 that
stabilizer in the lower range of abduction. However, the examined the effects of the glenohumeral capsule and
passive tension of the rotator cuff muscles was found not active musculature only. Our stud indicates that the
to affect inferior stability significantly.13<19 passive properties of the rotator cu lf may have a signif-
In this study, the rotator cuff carried large forces at icant effect on the stiffness of the joint as well.
all abduction angles tested in both the anterior and In conclusion, we have found that passive tension in
posterior directions and made a significant contribution the rotator cuff plays a significant role in stabilizing the
to the resisting force during application of an external glenohumeral joint during AP loading and should be
load. These results support our hypothesis and suggest considered in the treatment and diagnosis of gleno
that passive tension in the rotator cuff plays a signifi- humeral joint injuries, especially in the posterior direc-
cant role in the resistance of posterior loads when tion. In the future, the relative roles of the rotator cuff and
compared with the role of the other soft tissue structures glenohumeral capsule during internal and external rota-
at the glenohumeral joint. Even though previous studies tion will be examined in combination with AP loading.
applied comparatively smaller external loads
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