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Evaluation of the lag sign tests for external rotator function

of the shoulder
Christof Hurschler, PhD,a Nikolaus Wülker, MD,b Henning Windhagen, MD,a Niels Hellmers,a and
Piet Plumhoff,a Hannover and Tübingen, Germany

Rotator cuff lesions pose a serious clinical challenge. drop or lag sign tests (Figure 1,Table I); when the
The objective of this study was to verify the biome- patient is unable to hold an externally rotated posi-
chanical basis for the lag sign clinical tests for rotator tion, the resulting internal rotation, referred to as lag,
cuff dysfunction. The lag sign tests were simulated in indicates external rotator dysfunction. Tests per-
vitro by a sensor-guided robotic simulator configured formed at lower elevations have been proposed for
to reproduce in vivo testing conditions. The ability of the diagnosis of patients with shoulders too painful to
test at higher elevations.7
the test to isolate supraspinatus and/or infraspinatus
To be effective, tests of external rotator function are
dysfunction was investigated from 20° to 90° of scap- designed to minimize the confounding synergistic or
ular plane arm elevation. The test was 100% sensitive antagonistic effects of muscles other than those of
for lack of all infraspinatus–teres minor force at all ele- interest (such as the deltoid and pectoralis major).
vations tested (6/6 specimens at 20°, 30°, and 60° This attribute is confirmed by clinical, electromyo-
elevation; 5/5 at 90° elevation). The test was less sen- graphic (EMG), and biomechanical studies. EMG
sitive to complete loss of supraspinatus force (1/6 studies show that the SSP and ISP muscles are highly
specimens testing positive at 20°, 0/6 at 30°, 3/6 at activated in positions similar to those of the diagnostic
60°, and 3/5 at 90° elevation). The results of this bio- tests.9,12,13 Furthermore, biomechanical studies show
mechanical study suggest the lag sign tests to be that, in addition to the ISP, an external rotator, the SSP
highly sensitive only for infraspinatus–teres minor mus- muscle, also possesses an external rotation moment
arm in positions of external rotation.14 Thus, in posi-
cle dysfunction. (J Shoulder Elbow Surg 2004;13:
tions of external rotation, both the SSP and ISP can
298 –304.) contribute to the moment of external rotation.8,13
However, clinical investigations based on computed
C linical tests for rotator cuff function are designed to tomography arthrographic evaluation of muscle deg-
allow the examiner quickly and easily to detect pa- radation and/or intraoperative verification of tendon
thologies of the cuff muscles of the shoulder. Espe- ruptures remain inconclusive. The external rotation
cially important are tests used to diagnose partial and lag sign (ERLS) was thus found to be sensitive to
complete tears of the tendons of the external rotators, complete ruptures of the SSP independent of the con-
in particular of the supraspinatus (SSP) and infraspi- dition of the ISP in one study,7 whereas a test of
natus (ISP) muscles. These muscles are usually tested external rotational power in a similar position (0°
by assessing the patient’s ability to elevate the arm in abduction, 45° external rotation) was found to be
internal rotation,10 by evaluating the external rota- sensitive to stage 3 to stage 4 ISP fatty degeneration
tional power of the patient,6,12 or by assessing the in the presence of SSP and ISP tendon tears (length
ability of the patient to hold an externally rotated ranging from 2.5 to 5.0 cm).22 Fatty degeneration of
position.1 The latter tests have been referred to as the ISP has been shown to occur in the presence of
rotator cuff tears.5 Furthermore, although positions of
From the Department of Orthopaedic Surgery, Hannover Medical higher elevation are advocated for testing of the ISP,7
School, Hannover,a and Orthopaedic Clinics and Polyclinics, Walch et al22 found this position to be specific for the
University of Tübingen, Tübingen.b ISP only in combination with significant teres minor
This study was funded by the German Research Foundation (DFG). (TM) fatty degeneration.
Reprint requests: Christof Hurschler, PhD, Medizinische Hochschule It is thus not clear whether the lag sign tests for the
Hannover, Orthopädische Klinik, Annastift, Anne-von-Borries- rotator cuff can distinguish between ISP and SSP
Strasse 1-7, D-30625 Hannover, Germany (E-mail: hurschler@
annastift.de). ruptures and at what angles they should optimally be
Copyright © 2004 by Journal of Shoulder and Elbow Surgery tested. The goals of this study were, first, to measure
Board of Trustees. the sensitivity of the lag sign tests and, second, to
1058-2746/2004/$30.00 determine an optimal testing position for diagnosing
doi:10.1016/j.jse.2004.01.021 as well as differentiating defects of the SSP and ISP

298
J Shoulder Elbow Surg Hurschler et al 299
Volume 13, Number 3

Figure 1 A, Clinical examiner holding the test position for performing the ERLS test at 20° elevation, as described
in the text as well as in Table I. B, Photograph taken after release of the patient’s hand. Lag is defined as the amount
of internal rotation that occurs relative to the test position. A lag of greater than 5° is considered a positive test.

Table I Definitions of tests for external rotator function

Name Position Test criterion

Dropping sign 0° Abduction Forearm drops back to


(Walch et al,22 45° External rotation 0° external rotation
1998) 90° Elbow flexion
ERLS (Hertel et al,7 20° Elevation Angular drop or lag
1996) Max-5° External rotation recorded to nearest 5°
90° Elbow flexion
Drop sign (Hertel 90° Elevation Angular drop or lag
et al,7 1996) Max-5° External rotation recorded to nearest 5°
0° Elbow flexion

tendons of the rotator cuff. The clinical application of


the lag sign test was simulated in vitro with a sensor-
guided robot-assisted shoulder simulator. The method Figure 2 Photograph of shoulder specimen mounted in the simu-
used is unique because it allows simultaneous control lator, demonstrating the wires sutured to the SSP and ISP-TM
muscles, the humerus holder, the scapula mounting tower, the
of both the muscle forces (representing the patient manipulator end of the robot arm, and the FMS.
attempting to hold the test position) and the motion of
the specimen as it would be during the performance
of the clinical test (representing the examiner holding the rotator cuff were bluntly dissected away from the scap-
the elbow). The resulting internal rotation (ie, lag) that ula, and particular care was taken to preserve the integrity
occurred at different levels of ISP and SSP muscle of the joint capsule and ligaments as well as the rotator cuff
tendons and their insertions. Ductile wire was sutured to the
force over a range of elevation angles was precisely
musculotendinous junctions of the SSP, combined ISP and
measured in positions and under loading conditions TM (ISP-TM), and subscapularis (SSC) muscles to allow the
that closely mimicked those occurring during clinical application of muscle forces. Specimens were mounted in
evaluation. the testing machine (Figure 2) by use of 3 threaded steel
rods through the scapula according to a standardized
MATERIALS AND METHODS procedure as follows24: the scapula was first aligned with a
leveling gauge so that the tangent to the medial and inferior
Specimen preparation and mounting angles was vertically oriented. The plane of the scapula
Seven radiographically normal human shoulders (mean was then defined visually as the vertical plane passing
patient weight, 84 ⫾ 15 kg; mean age, 60 ⫾ 21 years, through both the medial and inferior angles of the scapula,
with three patients of unknown age) were harvested and as well as the middle of the glenoid surface. Finally, the
frozen before testing. The specimens were thawed at room scapula was tilted forward 10° to approximate its physio-
temperature for 12 hours before dissection of all muscles logic orientation on the thorax. The humerus was transected
except for the rotator cuff and deltoid. The muscle bellies of approximately 20 cm distal to the center of the humeral
300 Hurschler et al J Shoulder Elbow Surg
May/June 2004

Figure 4 Definition of all coordinate systems: tool coordinates of


the robot (T), measurement coordinates of the FMS (S), global
coordinate system fixed in space (G), and humeral coordinate
system at the geometric center of the humerus (H).
Figure 3 Schema of experimental setup illustrating the transfer of
the equivalent gravitational force (FEG) and moment (MEG) to the
IpeA, GmbH, Berlin, Germany) integrated into the control
geometric center of the humeral head, as well as the robot and FMS
to which the distal end of the humerus is attached. algorithm of the robot allowed it to function in real time
under force-moment control. Muscle force was applied by
computer-controlled hydraulic cylinders (accuracy of ⬍1
head and potted in a brass cylinder (outer diameter, 38 N).25 The force-moment sensor (FMS) measured the result-
mm; height, 5 cm) by use of cold-curing methyl methacrylate ant force and moment acting at the geometric center of the
resin (Technovit 4004; Heraeus Kulber, GmbH, Wehrheim, humerus (resolution ⬍3.0 N and ⬍0.15 Nm force and
Germany). The axis of the humerus was defined by aligning torsion, respectively; linearity ⬍1%). The robot (repeatabil-
the humerus and the cylinder with a specially designed jig ity of ⫾0.1 mm) and specially written control software were
inserted into the marrow cavity. The humerus was attached used to simulate the weight of the complete arm during the
to the robot by inserting the brass cylinder into a mount simulation (Figure 3).
attached to the force-moment sensor of the robot (Figure 2). The robot was programmed to permit motion only in the
Neutral rotation of the humerus was defined by palpation- same degrees of freedom as would the clinical examiner
aligning the intertubercular groove midway between the supporting the arm at the elbow and releasing the hand
coracoid process and the acromion. (internal-external rotation and medial-lateral and anterior-
posterior translation). The robot is, thus, not used in the
traditional sense (ie, to perform some predefined pro-
Simulation of clinical tests for external rotator function grammed motion) but rather as a device to apply loads and
The external rotator tests investigated in this study are control motions as they would occur during the clinical
applied clinically as follows7,22: the patient flexes the el- examination. The resultant equivalent gravitational force
bow to 90°, the arm is elevated in the scapular plane, and (FEG) and moment (M) vectors acting at the center of the
the examining clinician passively rotates the patient’s arm humeral head as a result of the weight of the arm were
to the maximum attainable externally rotated position while computed and superimposed on the load measured by the
holding the elbow (Figure 1, Table I). The actual position FMS (Figure 3). Anthropometric data for the upper arm,
tested is attained by derotating 5° to avoid excessive elastic forearm, and hand were used for these computations.21
recoil of the joint capsule (caused by tension in the anterior The robot was programmed to respond to the forces and
capsule). The test is defined as positive if the patient cannot moments acting on the specimen in a coordinate system that
hold this position and the arm rotates more than 5° inter- moved with the specimen (Figure 4). A continuously running
nally upon release of the hand (Figure 1, A and B). This test subroutine (Figure 5), with a turnaround time of 144 milli-
has been described at different arm elevations: when per- seconds or less between reading of FMS data and execu-
formed at 0° elevation, it is termed the dropping sign22; at tion of the motion commands, feedback-controlled the robot
20° elevation, it is termed the ERLS7; and at 90° elevation, (termed sensor-guided mode). This sensor-guided mode is
it is termed the drop sign7 (Table I). In this study the relative fast enough so that the resulting motion is perceived as a
contribution of the SSP and ISP muscles to both of these tests smooth motion. The FMS and humerus mount self-weight
was simulated in vitro at 20°, 30°, 60°, and 90° elevation were compensated so that they did not affect the measure-
in the scapular plane. The scapulothoracic-to-glenohumeral ment of force on the specimen.
angle relationship was assumed to vary according to Pop- The humeral coordinate system, located at the geometric
pen and Walker16 so that the corresponding glenohumeral center of the humeral head, was defined such that it was
angles were assumed to be approximately 16°, 22°, 33°, congruent with the global coordinate system when the
and 50°, respectively. specimen was centered in the glenoid and hanging under
The robot-assisted shoulder simulator used in this study its own weight in the previously defined position of neutral
(Figures 2 and 3) consisted of a previously described in rotation (Figure 4). The X-axis of the humerus thus corre-
vitro dynamic shoulder model24,25 combined with a sensor- sponded to the anatomic flexion-extension axis, the Y-axis
guided industrial robot (KR/15; Kuka, GmbH, Augsburg, corresponded to the axis of internal-external rotation, and
Germany). A 6-component force-moment sensor (KMS-60; the Z-axis corresponded to the axis of abduction-adduction.
J Shoulder Elbow Surg Hurschler et al 301
Volume 13, Number 3

the rotational axis of the humerus. This torque was chosen


based on preliminary experiments; it was high enough to
produce repeatable results while not damaging the speci-
men. To avoid excessive elastic capsular recoil, the test
position was finally obtained by derotating the arm 5°,
corresponding to the procedure recommended for the clin-
ical test.7
As a basis for investigating the relative contributions of
the SSP and ISP-TM muscles, normal SSP force and ISP-TM
force were determined as follows: the basic SSC antago-
nistic force was set at the level defined above for each
individual specimen, and SSP force and ISP-TM force were
increased proportionately according to their respective
physiologic cross-sectional areas (29.5% for SSP and
Figure 5 Flowchart of the algorithm used to control the robot. The 70.5% for ISP-TM)21 until the test position was maintained
resultant equivalent gravitational force (F) and moment (M) acting upon release of the arm. This was done at each elevation
on the specimen are measured by the FMS. The data are corrected angle tested. The muscle forces thus obtained (SSP, ISP-TM,
for the self-weight of the sensor and humerus-mounting bracket. The and SSC) were considered representative of those in a
force and moment vectors resulting from the weight of the arm are normal patient actively holding the test position and were
then computed (as a function of humerus position) and added to the
thus used to define 100% SSP and ISP-TM force.
measured values, which are subsequently translated into the ap-
propriate motion commands. The relative contributions of the SSP and ISP-TM force in
holding the test position were then investigated by chang-
ing the forces in the ISP-TM and SSP muscles and releasing
The term elevation used in this study refers to abduction in the arm from the test position. If the arm internally rotated
the scapular plane. more than 5°, the test was considered positive; if not, it was
The robot was used to simulate the boundary conditions negative. As the ISP and TM are considered the primary
during clinical examination (1) by blocking rotation about external rotators, force levels were chosen to range in
the humeral coordinate system X- and Z-axes (H in Figure 4), increments of 25% from 175% to 0% of normal for the SSP
preventing a change in flexion and elevation angles, re- and from 100% to 0% of normal for the ISP-TM. At each
spectively, and (2) by blocking translation along the global elevation angle investigated, a total of 15 combinations of
Y-axis (G in Figure 4), preventing superior-inferior transla- SSP and ISP-TM force were tested in a randomized order
tion. All other degrees of freedom—that is, anterior-poste- (Table II). Two-tailed paired Student t tests were used to
rior, superior-inferior, and medial-lateral translation—re- compare means at a significance level of ␣ ⫽ 0.05.
mained unconstrained. Muscle forces applied to the
tendons of the rotator cuff were simulated by 1.0-mm diam-
RESULTS
eter stainless steel cables routed over pulleys to computer-
regulated force-controlled hydraulic cylinders.25 The cables The results of the lag sign simulations are tabulated
were attached with wire suture and oriented to approximate according to the number of positive tests versus the
the anatomic lines of action of the muscles as closely as
possible: for the SSP through the SSP fossa; for the ISP-TM
number of specimens tested at each elevation angle
along the ISP fossa, bisecting the angle between the spine and combination of SSP and ISP-TM force tested
and the lateral margin of the scapula; and for the SSC (Table II). One of the seven specimens tested was
along the SSC fossa, also bisecting the angle between the removed from the series because it exhibited unusual
superior and lateral margins. laxity and an extreme external rotation of 104° at 90°
elevation, and thus almost no SSP and ISP-TM force
Experimental protocol was required to hold the test position. The SSP tendon
Physiologic cross-sectional areas of the individual mus-
insertion of another specimen failed at 90° elevation,
cles were used as a basis for determining muscle forces reducing the number of specimens tested to 5 at that
used in this simulation.4,15,18,20,21 Antagonistic SSC ten- elevation.
sion was first determined, and the ISP-TM force and SSP In general, the results showed that the force of both
force necessary to hold the test position were subsequently the SSP and ISP-TM muscles can affect the outcome of
determined as follows: minimum tension of the rotator cuff the lag sign tests. Decreasing the amount of ISP-TM
necessary to prevent the arm from subluxing under its own muscle force from 100% to 75% while holding SSP
weight was found by increasing the force on the SSP, force constant at 100% resulted in a clear rise in the
ISP-TM, and SSC proportionally (16.7% for SSP, 39.9% for number of positive tests: further reducing ISP-TM force
ISP-TM, and 43.3% for SSC)21 until the arm was held
to 50% or less resulted in all specimens testing posi-
stabilized in the glenoid. The lag sign test position at each
elevation angle was attained by elevating the arm in the tive (Table II). Decreasing SSP force while holding
scapular plane and maximally passively externally rotating ISP-TM force at 100% also resulted in an increase in
the arm while centering the humerus in the glenoid with a the number of positive tests; however, the effect was
20-N force. Maximum external rotation was defined as the less dramatic than with the ISP-TM and was almost
rotation at which a torque of 1.8 Nm was measured about nonexistent at 20° and 30° elevation (Table II). Thus,
302 Hurschler et al J Shoulder Elbow Surg
May/June 2004

Table II Number of positive lag Sign tests at indicated elevation angle and combination of SSP and ISP-TM force

SSP force

ISP-TM force 0% 25% 50% 75% 100% 125% 150% 175%

20° Elevation (N ⫽ 6)
0% — — — — 6 — — —
25% — — — — 6 — — —
50% — — — — 6 6 6 6
75% — — — 6 5 3 1 —
100% 1 0 0 0 0 — — —
30° Elevation (N ⫽ 6)
0% — — — — 6 — — —
25% — — — — 6 — — —
50% — — — — 6 5 5 4
75% — — — 4 3 3 2 —
100% 0 0 0 0 0 — — —
60° Elevation (N ⫽ 6)
0% — — — — 6 — — —
25% — — — — 6 — — —
50% — — — — 6 6 6 5
75% — — — 3 3 2 2 —
100% 3 1 1 0 0 — — —
90° Elevation (N ⫽ 5*)
0% — — — — 5 — — —
25% — — — — 5 — — —
50% — — — — 5 5 5 5
75% — — — 5 5 5 4 —
100% 3 2 2 1 0 — — —

The underlined zero indicates the level of force defined as the normal SSP and ISP-TM force sufficient to hold the test position (ie, 100% force). Cells
with dashes indicate force combinations that were not tested.
*One specimen was lost at 90° elevation because the SSP tendon tore at its insertion.

more than half of the tests were negative at all eleva- 50% ISP-TM force, the compensating effect of the SSP
tions tested despite the fact that all SSP force had is overwhelmed: increasing SSP force to 175% re-
been removed. This indicates that in some specimens, sulted in no increase at 20°, two additional positive
100% ISP-TM force alone is sufficient to hold the test tests at 30°, only one additional positive test at 60°,
position, whereas the inverse is not true—that is, and no increase at 90°.
100% SSP force alone is never sufficient to hold the
test position in the absence of ISP-TM force. DISCUSSION
The total amount of SSP and ISP-TM force required
to hold the test position increased with elevation The results of this study suggest that it is difficult to
angle from 114.5 ⫾ 25 N at 20° elevation to 171.4 distinguish between deficiencies of the SSP and
⫾ 54 N at 90° elevation (P ⫽ .051) (Figure 6). This ISP-TM muscles by use of the lag sign tests based on
increase occurred despite the fact that the antagonis- biomechanical considerations alone. Whereas com-
tic SSC force used for a particular specimen (mean, plete loss of ISP-TM force would result in 100% sen-
36.3 ⫾ 9 N) was held constant for all elevations sitivity at all elevations tested (Table I, 100% SSP
tested. The maximum external rotation attained also force), complete loss of SSP force would be more
increased with elevation angle from 68.3 ⫾ 18° at difficult to detect, especially at lower elevations. Al-
20° elevation to 81.3 ⫾ 22° at 90° elevation (P ⫽ though increasing with elevation, sensitivity for the
.004) (Figure 7). isolated SSP rupture was still only 50% (3/6) at 60°
Although the test is more sensitive to ISP-TM than
and 60% (3/5) at 90° elevation (Table II, 100%
SSP force, sensitivity to SSP force is increased when
ISP-TM force). The increased sensitivity to SSP force at
ISP-TM force is reduced, particularly at lower eleva-
higher elevation is a result of the increase in total SSP
tions. Thus, at 75% ISP-TM force, an increase of SSP
force to 150% results in fewer positive tests, particu- and ISP-TM force required to hold the test position
larly at 20° elevation, where four fewer positive tests with increasing elevation angle. The increasing force
were observed (Table II). This effect is smaller at 30°, required to hold the test position at increasing eleva-
60°, and 90° elevation, with one fewer positive test at tion is itself due in part to the increasing internal
each elevation angle, respectively. Furthermore, at rotational torque due to the weight of the arm, as well
J Shoulder Elbow Surg Hurschler et al 303
Volume 13, Number 3

system are multiple, limitations characteristic of all in


vitro simulations still apply. Muscle forces were simu-
lated by use of cables attached to the muscle-tendon
junctions of the combined ISP and TM, SSP, and SSC
muscles. Although the cables were oriented along the
physiologic axis of the muscle, the simulation of mus-
cles that may have more than one functional unit as a
single force is an inherent limitation of this and similar
studies.2,11,17,19 Although it has a small external
rotational moment arm,14 the deltoid muscle was not
simulated; its external rotational power is minimal
because of the externally rotated position in which the
test is performed. Furthermore, any external rotational
Figure 6 Total external rotator force of the SSP and ISP-TM muscles power of the deltoid would reduce even further the
required to hold the test position at each elevation angle tested. ability of the lag sign test to detect isolated SSP
ruptures. Finally, the ISP and TM muscles were simu-
lated as one functional unit. Although this assumption
is supported by EMG studies in normal patients,9
which indicate similar parallel activation patterns for
both muscles, observations of TM muscle hypertrophy
suggest that the TM may compensate for the reduced
external rotating power resulting from ISP tendon
tears.22 A strengthening of the TM would not contra-
dict the conclusions of this study, because it would
only serve to mask further the contribution of the SSP
muscle to external rotation strength.
It was impractical to simulate tendon ruptures di-
rectly by actually cutting the tendon, as we wanted to
investigate different combinations of SSP and ISP-TM
deficiency and the number of specimens available for
this study was limited. Dysfunction of tendon-muscle
Figure 7 Maximum external rotation attained at each elevation
angle tested. The test position is defined as the maximum externally
units was thus simulated by reducing force compared
rotated position minus 5° of internal rotation. with the 100% force, defined as the force required to
hold the test position and based on physiologic cross-
sectional areas. Significant superior glenohumeral
as the reducing rotational moment arm of the ISP, translation may occur in some patients with advanced
which occurs with increasing elevation.14 rotator cuff disease. The changes in muscle moment
The sensor-guided robot-assisted simulator used in arms that may result from such translations were not
this study differs from previous joint-kinematic investi- taken into consideration.
gations using industrial robots,3,23 primarily because Although we tested the ISP and TM as one func-
it was designed to evaluate both active and passive, tional unit (ISP-TM), the results of this study agree with
not just passive, structures of the joint. On the one those of Walch et al,22 who found a test performed at
hand, the system’s ability to move passively and 0° elevation and 45° external rotation to be positive
precisely measure the movement of the arm allows only in the presence of significant ISP degeneration in
noninvasive definition of a humeral coordinate system patients with combined tears of the SSP and ISP
at the geometric center of the humeral head. On the tendons. The authors suggested that, although exhib-
other hand, the ability to measure load and control iting a tear in the ISP tendon, patients without signif-
motion relative to a humeral coordinate system per- icant fatty degeneration retain enough ISP function to
mits simulation of the effect of the weight of the arm at pass the test.22 This hypothesis is supported by our
any position and orientation of the specimen. Finally, study, which indicates that, at lower elevation, less
and most importantly, the ability to allow or constrain force is required to hold the test position and that
motion freely in translation or rotation in any direction partial defects may be compensated by the other
of the global (fixed) or humeral (moving) coordinated muscles.
systems allows realistic simulation of the boundary The clinical study of Hertel et al7 found the lag sign
conditions imposed on the joint during the perfor- test at 20° elevation (ERLS) to be sensitive to ruptures
mance of the clinical lag sign test. of the SSP tendon, despite the presence of an intact
Although the advances and advantages of this ISP tendon. The results of our study suggest that it
304 Hurschler et al J Shoulder Elbow Surg
May/June 2004

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