Download Multi-axis passive and active stiffnesses of the glenohumeral joint

Clinical Biomechanics 19 (2004) 107–115
www.elsevier.com/locate/clinbiomech
Multi-axis passive and active stiffnesses of the glenohumeral joint q
Mohsen Makhsous, Fang Lin, Li-Qun Zhang
*
Department of Physical Medicine & Rehabilitation, Northwestern University, Chicago, IL, USA
Department of Orthopaedic Surgery, Northwestern University, Chicago, IL, USA
Department of Biomedical Engineering, Northwestern University, Evanston, IL, USA
Rehabilitation Institute of Chicago, 345 E. Superior Street, Room 1406, Chicago, IL 60611, USA
Received 25 September 2003; accepted 26 November 2003
Abstract
Objective. To investigate passive and active glenohumeral stiffness in the anterior, posterior, superior, and inferior directions at
different lateral positions of the humerus.
Design. Glenohumeral stiffness along multiple axes was determined in fresh-frozen shoulder specimens under both passive (no
simulated muscle contraction) and active (with simulated muscle contraction) conditions.
Background. Glenohumeral laxity has been evaluated in various studies with focus on one of the multiple directions. However,
glenohumeral stiffness characterizing the force–displacement relationship and stability has not been evaluated in all four directions
under passive and active conditions.
Methods. The humeral head was translated in the posterior, anterior, inferior and superior directions relative to the glenoid with
different lateral positions, and multi-axis glenohumeral stiffness generated by passive and active structures were investigated.
Results. Without muscle loading, glenohumeral stiffness in the superior direction (Ksup ¼ 5:83 N/mm) was higher than that in the
inferior (Kinf ¼ 4:32), anterior (Kant ¼ 3:67), and posterior (Kpost ¼ 2:89) directions (P < 0:008), and Kinf was higher than Kpost
(P ¼ 0:011). Stiffness in the different directions were correlated to each other (P < 0:001), and shifting the humerus laterally increased stiffness in all directions (P < 0:05) except for the superior direction. With moderate muscle loads, the glenohumeral joint
became significantly stiffer in all four directions (P < 0:05) with less difference among different directions.
Conclusions. Glenohumeral stiffnesses are different in the different directions but are correlated to each other and contribute
jointly to glenohumeral stability. Muscle contractions can increase glenohumeral stiffness significantly.
Relevance
Multi-axis glenohumeral stiffness characterizes glenohumeral stability in 3D space and is related to glenohumeral functional
movement that always involves multiple directions. The approach provides us a quantitative tool to evaluate shoulder biomechanical properties, and similar method can potentially be used in vivo on human subjects to assess shoulder injuries and treatment
outcome.
Ó 2003 Elsevier Ltd. All rights reserved.
Keywords: Glenohumeral joint; Stiffness; Stability; Shoulder; In vitro
1. Introduction
The glenohumeral (GH) joint is one of the most
mobile joints of the human body with the humeral head
supported partially by the relatively small concave gle-
q
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.clinbiomech.2003.11.009
*
Corresponding author.
E-mail address: [email protected] (L.-Q. Zhang).
0268-0033/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.clinbiomech.2003.11.009
noid. Passive structures, including the joint capsule,
ligaments, labrum and articular surfaces, function together with muscles crossing the GH-joint to maintain
stability of it (Soslowsky et al., 1997). One or more of
the structures may be injured in various shoulder
problems, resulting in altered GH stability and stiffness
in the anterior, posterior, superior, and/or inferior
directions (Soslowsky et al., 1997; Halder et al., 2001a;
Blasier et al., 1997; Weiser et al., 1999; Ticker and
Warner, 2000; Debski et al., 1999b; Warner et al., 1992;
McQuade et al., 1999).
108
M. Makhsous et al. / Clinical Biomechanics 19 (2004) 107–115
GH-joint stability and laxity have been assessed by
evaluating the resistance and/or range of motion during
passive manual movement (Soslowsky et al., 1997;
Halder et al., 2001a; Blasier et al., 1997; Weiser et al.,
1999; Ticker and Warner, 2000; Debski et al., 1999b;
Warner et al., 1992; McQuade et al., 1999). Since the
measured joint laxity depends on the force applied, joint
stiffness that characterizes the relationship between the
force and displacement avoids such dependence and
provides us an objective measure of the joint stability,
independent of the load applied by an examiner. Clinically, GH stiffness may be changed considerably in
shoulder injuries. On the one hand, the GH-joint may
become too compliant with much reduced joint stiffness
in unstable shoulders. On the other hand, a joint may
become too stiff with severely reduced the range of
motion in cases like frozen shoulders.
GH instabilities occur in various directions of the
GH-joint. A number of studies have been conducted to
determine how different capsuloligamentous structures
and muscles contribute to GH laxity, with each study
generally focused on only one or two specific anatomical
directions, such as the inferior (Soslowsky et al., 1997;
Halder et al., 2001a), posterior (Blasier et al., 1997),
anterior (Weiser et al., 1999; Ticker and Warner, 2000),
posterior–anterior (Debski et al., 1999b; McQuade
et al., 1999), inferior–superior (Warner et al., 1992) or
anterior–inferior directions (Ticker and Warner, 2000;
Malicky et al., 2001). It is not clear how different
structures contribute to GH stability in the various
anatomical directions (anterior, posterior, inferior and
superior) in the same specimens, although GH stability
along the multiple axes are related to each other and
shoulder functions always involve multi-axis GH
movement. There is also a lack of information on the
dependence of GH stability on the humeral lateral position relative to the glenoid. Therefore, characterizing
GH-joint stiffness along the multiple anatomical directions, and at different lateral humeral positions in the
same specimens is useful to understand and evaluate
GH-joint stability and functional performance in 3D
space.
The purpose of this study was to investigate contributions of capsuloligaments and muscle-tendon complexes crossing the GH-joint to GH stiffness along four
anatomical axes of the glenoid (rather than only along a
single direction). The hypotheses were: (1) GH capsuloligaments stiffness in the superior (Ksup ), inferior (Kinf ),
anterior (Kant ), and posterior (Kpost ) directions are different from each other in amplitude but are correlated to
each other; (2) lateral shift of the humerus increases GH
stiffness in all four directions; (3) moderate loading of
muscles crossing the GH-joint increases the joint stiffness significantly in all four directions. Study of passive
and active control of GH-joint will help us better
understand biomechanics of the GH-joint in 3D space,
which may help us evaluate shoulder injuries, surgical
outcome, and rehabilitation progress more accurately.
Quantitative measure of GH stiffness along multiple
axes may also help us improve existing computer
shoulder models by providing characterization of GH
stiffness/stability associated with GH translations that
have been neglected in existing models and the joint is
assumed to have only three rotational degrees of freedoms (a ball-socket joint).
2. Methods
Specimen: Six fresh-frozen shoulder specimens (three
left and three right specimens) from five cadavers with
no sign of injury were used in the study. The donors
were on average 56.83 (SD 3.43) years old at death and
all of them were male. After peeling off the skin and
subcutaneous tissues, the anterior, medial, and posterior
portions of the deltoid, supraspinatus, teres minor, long
head of biceps, upper, middle, and lower portions of the
subscapularis and infraspinatus were dissected and
separated from each other. A cable was sutured to each
of the individual muscles through fiberglass mesh
wrapped around the proximal end of the muscles except
for the long head of biceps, which was loaded at the
distal end. Each portion of the muscles was loaded along
its line of action through a pulley system. The posterolateral corner and inferior part of the anterolateral of
the acromion was chopped off to eliminate acromiohumeral impingement during the passive movement.
Furthermore, potential impingement was checked by
visual inspection and by monitoring possible sharp rise
of the restraining force during the passive movement.
Experimental setup: The specimen was mounted on a
custom designed testing device, which allowed three
rotations (abduction–adduction, flexion–extension, and
internal–external rotation) and three translations (posterior–anterior, inferior–superior, and medial–lateral) of
the humerus relative to the glenoid (Fig. 1). The scapula
was bolted rigidly onto a Teflon plate with the glenoid
surface oriented vertically. The humerus was fixed into
an aluminum tubing by sharpened screws and the shaft
of humerus was aligned with the centerline of the tubing.
The arm was positioned at 60° GH abduction in the
scapular plane. The aluminum tubing was attached to a
beam parallel to the humeral shaft (Fig. 1). The beam
was in turn mounted to an X –Y table controlled by two
micrometers, which allowed adjustment of the humerus
relative to the glenoid in the posterior–anterior and
proximal–distal directions. The X –Y table was fixed to
the bench through a six-axis force sensor (JR3 Inc.,
Woodland, CA, USA), which was aligned with the axes
of the humerus coordinate system (Fig. 1). The scapula
could be translated in the medial–lateral and inferior–
superior directions by another X –Y table. The dis-
M. Makhsous et al. / Clinical Biomechanics 19 (2004) 107–115
Fig. 1. Experimental setup: The scapula was bolted onto a plate with
the glenoid surface oriented vertically. The arm was positioned at 60°
GH abduction in the scapular plane. An X –Y table allowed adjustment
of the humerus relative to the glenoid in the posterior–anterior and
proximal–distal directions. The X –Y table was fixed to the bench
through a six-axis force sensor (JR3). Another X –Y table was used to
translate the scapula in the medial–lateral and inferior–superior
directions. The displacements of the two X –Y tables were measured by
four linear potentiometers. Three precision rotary potentiometers were
used to measure the humeral abduction, flexion, and axial rotation.
placements of the two X –Y tables were measured by
four linear potentiometers (Midori America Co., Fullerton, CA, USA) as well as by the micrometers built
into the X –Y tables. The humeral abduction, flexion,
and axial rotation were measured by three precision
rotary potentiometers. The six-axis force sensor was
used to measure the restraining forces and moments
exerted onto the humerus caused by translations of the
humerus relative to the glenoid (Fig. 1).
Glenoid coordinate system: Anatomical axes were defined to be in line with the posterior–anterior (X ), inferior–superior (Y ), and medial–lateral (Z) axes of the
glenoid coordinate system (Fig. 2). The þY -axis was
directed superiorly from the most inferior edge of the
glenoid to the biceps long head origin (Novotny et al.,
2000), and þX -axis pointed anteriorly perpendicular to
the þY . The þZ-axis pointed laterally for the right
shoulder and medially for the left shoulder and perpendicular to the X and Y axes. The origin of the
coordinate system was located at the center of the
humeral head.
Protocol: Before dissecting the shoulder specimen
with all muscles intact, the anatomical neutral position
of the humeral head was measured by digitizing landmarks on the humerus and scapula using a digitizer
(MicroScribe-3D, Immersion Corp., CA, USA), with
the arm positioned at 60° GH abduction in the scapular
plane. The landmarks were marked by inserting small
pins into the bony landmarks. The following bony
landmarks were chosen for the scapula and humerus:
The most superior point of the acromio-clavicular joint,
angulus inferior, angulus superior, angulus acromialis,
and trigonum spinae on scapula, and the epicondylus
109
Fig. 2. Anatomical axes of the glenoid coordinate system for the right
shoulder. The þY -axis is directed superiorly from the most inferior
edge of the glenoid to the long head of biceps origin, and þX -axis
points anteriorly perpendicular to the þY -axis. The þZ-axis points
laterally for the right shoulder. The origin of the coordinate system is
located at the center of the humeral head. The humerus coordinate
system (XH ; YH ; ZH ), which was aligned with the force-sensor coordinate system was also given here.
medialis, epicondylus lateralis and one arbitrary point
on the humeral shaft. After separating the muscles, the
center of the humeral head was aligned with the center
of glenoid as follows: First, the humeral head was
pressed manually by about 20 N compressive load into
the glenoid fossa to ensure concentric reduction of the
humeral head in the socket (Hawkins and Bokor, 1990)
and the compressive load was then released to let the
humeral head back to the neutral medial–lateral position; second, the neutral axial rotation of the humerus
was located by positioning the bicipital groove about
45° externally rotated relative to the scapular plane and
close to the mid-point between full passive internal and
external rotation (Warner et al., 1992); third, the above
mentioned digitized data was used to correct any malalignment of the humeral head at the neutral position by
using the orientation of the local coordinate systems
including the absolute distance between the origins of
these systems. After experiment, additional landmarks
on the humeral head and glenoid surface were digitized
to define the local coordinate systems for the humerus,
scapula and glenoid (Makhsous, 1999). In selected
specimens, the humeral head center was defined by fitting a hemisphere to the humeral head. Before the
testing, the shoulder was elevated up and down about 20
times to minimize the viscoelastic effect of the soft tissue.
Restraining forces were measured statically when the
humerus was translated relative to the glenoid in the
posterior–anterior (X ¼ 16 to 16 mm) and inferior–
superior (Y ¼ 10 to 5 mm) directions by adjusting the
micrometers at the increment of 4.0 (i.e. X ¼ 16, )12,
)8, )4, 0, 4, 8, 12, 16 mm; a total of nine data points),
and 2.5 mm (i.e. Y ¼ 10, )7.5, )5, )2.5, 0, 2.5, 5 mm; a
total of seven data points), respectively, at a fixed lateral
translation (Z ¼ 0, 2.5, 5 mm) in the neutral position of
the humeral head. In this way 9 7 ¼ 63 data points
110
M. Makhsous et al. / Clinical Biomechanics 19 (2004) 107–115
were collected in a posterior–anterior/inferior–superior
plane at each fixed lateral position. The order of translation of the humerus along the X and Y axes was
randomized at a fixed Z translation. A period of 10 s
between two consecutive positions was used to minimize
the hysteretic effect of the capsuloligamentous structure
during the passive movement. The restraining force was
monitored during the passive translations to avoid
excessive loading of the joint structure. The experimental protocol was tested using two shoulder specimens in order to find appropriate initial position. It was
also tested to find reasonable range of translations along
the anatomical axes.
In order to evaluate contributions of the passive GH
capsuloligamentous structure and active muscle tone
contraction to joint stability, the test was repeated with
no muscle load (Passive condition) and with 1% maximum muscle force on all muscles or muscle portions
proportional to the muscle physiological cross-sectional
area (PCSA) (Active condition) (Makhsous, 1999;
Morrey and An, 1990), representing the physiological
muscle tone contraction (Basmajian and De Luca, 1985;
Makhsous et al., 1998; Walsh, 1992) during free arm
suspension. For the calculation of the PCSA for individual specimen, we used a set of PCSA (Makhsous,
1999) (Table 1).
Data analysis: Forces and moments were transformed
from the force-sensor coordinate system into the glenoid
coordinate system with components in the posterior–
anterior (X ), inferior–superior (Y ) and medial–lateral
(Z) directions.
Force vector fields were used to characterize the
direction and magnitude of the restraining forces applied to the humeral head by the GH capsuloligamentous structure and muscles during the passive
movement. At each GH position, shear force measured
in the posterior–anterior/inferior–superior (sagittal or
X –Y ) plane was illustrated by small arrows with the
length and direction corresponding to the force magnitude and direction, respectively.
Table 1
The muscle forces (N), mean (SD)
Muscle
1% maximal muscle force (N)
Deltoid Ant.
Deltoid middle
Deltoid Post
Teres minor
Long head of biceps
Upper subscapularis
Middle subscapularis
Lower subscapularis
Upper infraspinatus
Middle infraspinatus
Lower infraspinatus
Supraspinatus
6.68
5.28
6.20
2.36
3.28
3.26
3.35
4.59
4.33
4.30
4.66
3.28
(2.10)
(3.22)
(0.02)
(0.55)
(0.25)
(1.80)
(1.05)
(1.44)
(1.80)
(1.39)
(1.71)
(0.25)
The 1% maximal muscle forces (N) for each of the shoulder muscles
are based on the data from Makhsous (1999).
Stiffness of the GH capsuloligamentous structure and
muscles crossing the GH-joint, defined as the ratio of the
incremental force required to stretch the passive/active
structures over a range of translation (Ki ¼ DFi =DTi ,
i ¼ (post, ant, inf and sup)), was calculated for each
direction of translations starting from the neutral position. A least square regression was used to calculate the
slope of the fitted line to the collected data points for
each direction of translation.
The line of action of the shear force (F) exerted onto
the humeral head in the sagittal plane of the glenoid
coordinate system was characterized by the directional
cosine (DC) as follows:
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
Fx
Fy
DCx ¼ ; DCy ¼ ; FS ¼ Fx2 þ Fy2
FS
FS
where FS is the magnitude of the shear force, and Fx and
Fy are the restraining force components applied to the
humerus along the glenoid X and Y axes, respectively
(Zhang et al., 1998). Considering the 3D total restraining force (FT ), the corresponding directional cosines
(DCTx , DCTy , DCTz ) are determined.
Fx
Fy
DCTx ¼ ; DCTy ¼ ;
FT
FT
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
FT ¼ Fx2 þ Fy2 þ Fz2
DCTz ¼
Fz
;
FT
A mixed effect model was used to test the hypothesis
that GH stiffness (the response variable) in the anterior,
posterior, superior, and inferior directions are not statistically different (P R O C M I X E D , SAS statistical software package). The main effect of direction (the
anterior, posterior, superior, and inferior) was assessed
in a random effects model that accounted for specimen
as a random effect. Stiffness in the different directions
from the same specimens was treated as paired samples
in the analysis. The Bonferroni correction method was
used to adjust the level of statistical significance for
testing six pairwise multiple comparisons. This method
was also used to test whether muscle loads increased
stiffness along each of the four directions, based on
paired samples in the specimens. Paired t-test was used
to compare the stiffness in each direction between with
and without muscle loading conditions. To evaluate the
correlation between the GH stiffness at different directions (Kant , Kpost , Kinf and Ksup ), Pearson’s productmoment correlation coefficients (PCC) were calculated
between each pair of the directions over all specimens.
3. Results
Passive condition: The restraining force varied systematically with the passive posterior–anterior and
inferior–superior translations (Fig. 3). The capsuloligaments generated considerable restraining forces at the
M. Makhsous et al. / Clinical Biomechanics 19 (2004) 107–115
27% (P ¼ 0:018), 23% (P ¼ 0:049), 10% (P ¼ 0:054) and
8% (P ¼ 0:049) in the posterior, superior, inferior and
anterior directions, respectively (Table 3). Multiple
comparison of the stiffness between each pair of directions showed that Ksup was significantly higher than Kpost
(P ¼ 0:002), Kant (P ¼ 0:002), and Kinf (P ¼ 0:032) at
5 mm lateral translation.
Shifting the humerus superiorly with Sup ¼ 5 mm and
Lat ¼ 0 mm increased Kpost and Kant significantly by 21%
(P ¼ 0:021) and 18% (P ¼ 0:026), respectively. On the
other hand, shifting the humeral head inferiorly
(Inf ¼ 10 and Lat ¼ 0 mm) significantly increased only
Kpost by 30% (P ¼ 0:028). With the humeral head at
the extreme anterior translation (Ant ¼ 16 mm) Ksup
increased 31% (P ¼ 0:031).
extreme translations (Table 2). At the extreme translations, the restraining force pointed along the line of
passive translation and towards the neutral position, as
indicated by the DCx and DCy (Table 2).
The restraining force generated by the capsuloligaments increased linearly (Fig. 4(a) and (b)), indicating
constant stiffness (slope of the force–displacement
curve). Translating the humeral head superiorly resulted
in the highest resistance force and stiffness (P < 0:008)
among all the directions. Kinf and Ksup at the zero
anteroposterior and lateral translations were higher than
Kpost and Kant at the zero superior–inferior and lateral
translations (Fig. 4(c) and (d) and Table 3).
When the capsuloligaments were stretched laterally
by 5 mm, the stiffness of the capsuloligaments increased
Inf - Sup (mm)
Passive
Lat = 0
Y
5
X
0
-5
-5
-10
Active
Y
5
0
-10
111
X
-10
0
10
-10
0
10
Post-Ant(mm)
Post-Ant(mm)
Contour(10, 20,...N)
Fig. 3. Representative restraining force field as a function of posterior–anterior (X -axis) and inferior–superior (Y -axis) translations and at Lat ¼ 0 mm
for the passive, and active conditions. The contour lines are given at 10; 20; 30; . . . N for force field diagrams. The dots indicate the rim of the glenoid
surface. The origin in the force field corresponded to the neutrally aligned position between the humeral head and glenoid. The arrows represent the
resistance forces induced by the passive displacements. The length and direction of the arrows represent the magnitude and direction of the resistance
force, respectively.
Table 2
The magnitude of shear force (FS ) and the corresponding directional cosines (DCx and DCy ) in Mean (SD)
Load condition
Position (mm)
FS (N)
Passive
Lat ¼ 0
Ant ¼ 16
Post ¼ 16
Sup ¼ 5
Inf ¼ 10
Ant ¼ 16, Sup ¼ 5
Post ¼ 16, Sup ¼ 5
Ant ¼ 16, Inf ¼ 10
Post ¼ 16, Inf ¼ 10
34.9
34.9
46.1
38.6
57.1
52.9
51.1
54.3
(23.3)
(16.6)
(17.3)
(15.5)
(20.5)
(18.4)
(21.0)
(16.5)
Lat ¼ 0
Ant ¼ 16
Post ¼ 16
Sup ¼ 5
Inf ¼ 10
Ant ¼ 16, Sup ¼ 5
Post ¼ 16, Sup ¼ 5
Ant ¼ 16, Inf ¼ 10
Post ¼ 16, Inf ¼ 10
53.8
52.5
50.9
47.9
76.2
71.0
75.0
70.5
(19.2)
(29.1)
(26.6)
(14.5)
(19.1)
(17.3)
(16.5)
(14.6)
Active
P
0.003
0.069
0.165
0.132
0.029
0.036
0.023
0.008
DCx
DCy
)0.96
0.94
0.09
)0.13
)0.68
0.68
)0.84
0.65
(0.07)
(0.06)
(0.24)
(0.14)
(0.23)
(0.22)
(0.10)
(0.19)
)0.16
)0.07
)0.97
0.98
)0.63
)0.66
0.52
0.72
(0.16)
(0.38)
(0.04)
(0.02)
(0.12)
(0.28)
(0.16)
(0.19)
)0.96
0.96
0.05
)0.22
)0.80
0.75
)0.69
0.58
(0.05)
(0.04)
(0.22)
(0.20)
(0.16)
(0.11)
(0.07)
(0.10)
0.02
)0.17
)0.98
0.93
)0.50
)0.64
0.72
0.80
(0.24)
(0.28)
(0.03)
(0.09)
(0.12)
(0.13)
(0.06)
(0.08)
The FS , DCx and DCy exerted onto the humeral head at the extreme translations in the sagittal plane, i.e. anterior (Ant ¼ 16 mm), posterior (Post ¼ 16
mm), superior (Sup ¼ 5 mm), inferior (Inf ¼ 10 mm), anterosuperior (Ant ¼ 16, Sup ¼ 5 mm), posterosuperior (Post ¼ 16, Sup ¼ 5 mm), anteroinferior (Ant ¼ 16, Inf ¼ 10 mm) and posteroinferior (Post ¼ 16, Inf ¼ 10 mm), and at Lat ¼ 0 mm under the passive and active conditions. P -values
were given for differences between the passive and active load conditions.
M. Makhsous et al. / Clinical Biomechanics 19 (2004) 107–115
F (N)
112
80
40
0
-8 -400
8
-80
X (m m )
post
ant
-16
(a)
K (N/mm)
8
6
*
P<0.001
+
4
16
-10
-5
(b)
8
*
P<0.001
6
P=0.011
50
25
0
-25 0
-50
Y (mm)
inf
5
sup
*
P<0.008
+
*
4
2
2
0
Y=0
Kpost
(c)
0
Kant
(d)
X=0
Ksup
Kinf
Fig. 4. Representative force–displacement relationship of the GH-joint at Lat ¼ 0 mm: (a) in the anterior (þX ) and posterior (X ) directions at zero
superior–inferior translation (Y ¼ 0); (b) in superior (þY ) and inferior (Y ) directions at zero posterior–anterior translation (X ¼ 0). Passive stiffness
(over six specimens) at Lat ¼ 0 mm: (c) Kpost and Kant at the zero inferior–superior translation (Y ¼ 0 mm); (d) Kinf and Ksup at zero posterior–anterior
translation (X ¼ 0 mm). No muscle load was applied during the test. The P -values were given when the stiffness was compared to Ksup () or to
Kinf (+).
Table 3
GH-joint stiffness (K): mean (SD)
Loading conditions
(starting) (mm)
Kant
Kpost
Ksup
Kinf
Absolute
Change
Absolute
Change
Absolute
Change
Absolute
Change
(N/mm)
(%)
(P)
(N/mm)
(%)
(P)
(N/mm)
(%)
(P)
(N/mm)
(%)
(P)
–
–
0.049
0.026
0.278
2.89
3.66
3.50
3.76
–
27
21
30
–
0.018
0.021
0.028
5.83 (0.92)
7.18 (2.10)
–
23
–
0.049
4.32 (1.07)
4.77 (0.87)
–
10
–
0.054
7.65 (1.39)
7.77 (1.86)
31
33
0.031
0.080
4.52 (2.42)
5.26 (0.93)
5
22
0.419
0.067
6.81 (1.79)
7.47 (1.60)
17
10
0.048
0.029
4.93 (1.08)
5.67 (1.36)
14
15
0.047
0.174
8.32 (1.98)
7.77 (1.41)
22
14
0.031
0.138
5.60 (0.95)
5.59 (0.92)
13
13
0.083
0.039
Passive
Lat ¼ 0
Lat ¼ 5
Lat ¼ 0
Lat ¼ 0
Lat ¼ 0
Lat ¼ 0
(0)
(0)a
(Sup ¼ 5)a
(Inf ¼ 10)a
(Ant ¼ 16)a
(Post ¼ 16)a
3.67
3.97
4.32
3.85
Active
Lat ¼ 0
Lat ¼ 5
Lat ¼ 0
Lat ¼ 0
Lat ¼ 0
Lat ¼ 0
(0)a
(0)b
(Sup ¼ 5)b
(Inf ¼ 10)b
(Ant ¼ 16)b
(Post ¼ 16)b
4.32
4.32
4.50
4.31
(1.32)
(1.62)
(1.45)
(1.74)
(1.17)
(1.74)
(1.44)
(1.59)
8
18
5
18
0
4
0
0.026
0.496
0.139
0.489
3.60
4.02
3.62
3.99
(0.79)
(1.04)
(1.24)
(1.11)
(1.15)
(1.31)
(1.38)
(1.18)
24
12
1
11
0.014
0.076
0.442
0.050
The absolute values (N/mm; first column) and changes (%; second column) in the K for different loading conditions (passive and active), different
directions (the anterior, posterior, superior and inferior), and with the humeral head at the neutral position and at the extreme translations (Ant ¼ 16,
Post ¼ 16, Sup ¼ 5 and Inf ¼ 10). The starting position of the GH-joint is given under loading conditions, for example the 1st row shows the stiffness
values across the range of anterior, posterior, superior and inferior translations at fixed lateral displacement (Lat ¼ 0). The P -values were given when
the stiffness was compared to passive condition at Lat ¼ 0a or to active condition at Lat ¼ 0b .
a
Relative to passive condition at Lat ¼ 0.
b
Relative to active condition at Lat ¼ 0.
Active condition: Loading the muscles at 1% of their
maximal forces increased the restraining forces considerably, as indicated by the shrinkage of the contour
curves and the faster rise of the restraining forces with
the passive displacements (Fig. 3). Compared with the
passive condition, FS increased 54% (P ¼ 0:003), 34%
(P ¼ 0:029), 34% (P ¼ 0:036), 47% (P ¼ 0:023), and 30%
(P ¼ 0:008) in the anterior, anterosuperior, posterosuperior, anteroinferior, and posteroinferior directions
(Table 2), respectively. The FT at the active condition was increased by 62% (P ¼ 0:024) and 62% (P ¼
0:016) in the anterior and posterior directions, respectively.
Active tone contraction of muscles crossing the GHjoint increased Kpost , Kant , Ksup and Kinf significantly by
24% (P ¼ 0:014), 18% (P ¼ 0:026), 17% (P ¼ 0:048), and
14% (P ¼ 0:047), respectively, when the muscles crossing
the GH-joint were loaded (Table 3). Under the active
M. Makhsous et al. / Clinical Biomechanics 19 (2004) 107–115
condition, Ksup (6.81 N/mm) was significantly higher
than Kinf (4.93 N/mm, P ¼ 0:034), Kant (4.32 N/mm,
P ¼ 0:005), and Kpost (3.60 N/mm, P < 0:001). Laterally
stretching the capsuloligaments 5 mm with active muscle
loading increased Ksup by 10% (P ¼ 0:029). Ksup was
significantly higher than Kpost (P ¼ 0:002) and Kant (P ¼
0:005) (Table 3). Moving the humerus to the extreme
anterior and posterior positions increased Ksup by 22%
(P ¼ 0:031) and Kinf by 13% (P ¼ 0:039), respectively.
GH Stiffness in the different directions were (P <
0:001) correlated to each other significantly (Table S1
supplementary data). The GH stiffness under active
condition had significantly higher correlation (PCC >
93%) than that at the passive condition (PCC > 90%).
4. Discussion
The study provides us quantitative characterization
of the functionally relevant multi-axis stiffness provided
by the GH capsuloligamentous structures and active
structures along the posterior, anterior, inferior and
superior directions, and at different lateral humeral
positions. The multi-axis stiffness was evaluated in the
same shoulder specimens so that the stiffness properties
along different axes were closely matched to each other
for each shoulder specimen. GH stiffness in the superior,
inferior, anterior, and posterior directions are correlated
to each other but are different in amplitude. Evaluation
of stiffness in all four anatomical directions in the same
specimens closely matched the stiffness properties
among the different axes for each shoulder specimen,
which minimized the experimental error associated with
specimen variations and provides us a functionally relevant multi-axis characterization.
The 60° GH abduction at the neutral axial rotation
was chosen in this study, which was found to be a position with large GH laxity in all directions (Halder
et al., 2001a; Debski et al., 1999b; Warner et al., 1992;
Harryman et al., 1990). The translations used in the
experiment were not excessive. Even larger GH displacements ( P 20 mm) were used by some investigators,
which was believed not likely to damage the specimens
during repeated testing (Harryman et al., 1990; Helmig
et al., 1993). In addition to the reported lateral translations (Z ¼ 0, 2.5, 5 mm), the GH-joint was also
translated to Z ¼ 2:5 mm. The GH-joint could not be
translated more than 3–4 mm at this position due to
glenoid bony constraint. In order to avoid potentially
overloading the joint structure, the restraining force was
monitored during displacements in our study. The range
of peak resistance force (Fi ) observed at the extreme
position of the translations in the sagittal plane of the
glenoid surface in our study were 32–90 N, 28–80 N, 35–
62 N and 33–70 N for the anterior, posterior, superior
and inferior displacements, respectively.
113
Within the range of load tested, the resistance force
increased approximately linearly with the displacement
with the relationship characterized by the corresponding
stiffness. A linear relationship between the force and
displacement was reported previously during clinical
examination of the GH-joint (McQuade et al., 1999) and
during in vitro anterior–posterior loading of the GHjoint capsule (Debski et al., 1999b).
Larger translations and lower stiffness were observed
in the anterior–posterior directions than that in the
superior–inferior directions, possibly related to the
shapes of the glenoid and the labrum, which are more
curved in the superior–inferior direction than in the
anterior–posterior direction (McPherson et al., 1997).
In a study of stability ratios (Halder et al., 2001b), the
humeral head was found to be more stable in the
superior–inferior direction than in the anterior–posterior direction with the reason given as the deeper glenoid
labral concavity in the inferior–superior direction than
that in the posterior–anterior direction. Comparisons of
the stiffness in the posterior–anterior or inferior–superior axes indicated that the GH stiffness was higher in
the superior and anterior directions than that in the
inferior and posterior directions, respectively.
In a study of the static capsuloligamentous restraints
to superior–inferior translation, higher stability was
found in the superior direction than in the inferior
direction at three positions of GH abduction (0°, 45°,
90°) (Warner et al., 1992). The higher superior stiffness
of the capsuloligaments may be helpful in preventing the
impingement of the humeral head into the coracoacromial arch.
Compared with the passive condition at zero lateral
displacement, the stiffness was significantly increased for
all directions of translations with physiological load
indicating higher joint stability in all directions. Moreover, under active condition, no significant difference
was found among the GH stiffness in the inferior,
anterior and posterior directions. The stiffness increased
relatively more quickly where the passive joint stiffness
was relatively low, i.e. for Kpost (increased 24%) and Kant
(increased 18%). This was consistent with the previous
finding (Debski et al., 1999a) that the tension in the
muscles crossing the GH-joint increased significantly
more the posterior stability than the anterior stability.
The active condition used in this study resembled the
condition under which a clinical static stability test is
usually performed. In these tests, although the patient is
asked to be as relaxed as possible, the muscle tone always exists even without voluntary contraction (Matsen
et al., 1990). The results suggested that low-level muscle
activity, representing physiological muscle tone contraction, is important and effective in stabilizing the
GH-joint (Makhsous et al., 1998; Kumar and Balasubramaniam, 1985; Moseley and Overgaard, 1962;
Symeonides, 1972). The muscle tone contraction is
114
M. Makhsous et al. / Clinical Biomechanics 19 (2004) 107–115
difficult to measure and it is not available in the literature. A pilot study was done (Makhsous et al., 1998) to
identify muscle tone contraction with 90° and 45° of
humeral abduction in the scapular plane. The muscle
tone was found to be within 1–7% of the maximum
muscle contraction and in this study the lowest muscle
tone level was used. When the humeral head is translated laterally, the capsule and ligaments were stretched
as indicated by the higher GH stiffness (Table 3) and
restraining force (Table S2 supplementary data) for all
the direction.
Current established GH-joint models in the literature
usually allow unrestricted translations in the medial–
lateral direction when the humerus was moved in the
posterior–anterior or inferior–superior directions to
evaluate GH laxity (Halder et al., 2001a; Weiser et al.,
1999; Debski et al., 1999b). In this study, we took a
different approach and evaluated multi-directional GHjoint stiffness at several fixed medial–lateral positions,
with the multi-axis resistance force acted on the humeral
head by passive and active restraints measured by a sixaxis force sensor at a fixed medial–lateral position. In
other words, we measured the multi-axis resistance force
at controlled GH positions and used the force–displacement relationship to characterize the multi-axis
GH stiffness. To avoid excessive load to the glenoid, the
resistance force was limited/controlled to be within a
pre-specified range. Furthermore, the resistance force in
the medial–lateral as well as other directions at controlled GH positions provides useful information on the
stabilizing contributions of the passive and active
structures including the labrum and glenoid.
The study provided quantitative measures of the GH
stiffness in all anatomical directions obtained from the
same specimens. This helps us understand the roles of
the capsuloligaments and muscles in GH stability, analyze GH injury, and develop more accurate mathematical models of the GH-joint. A better understanding of
the different but interrelated passive and active GH
stiffness evaluated along multiple axes may help us
interpret the results of multi-axis laxity tests and evaluate shoulder laxity at different conditions. Low-level
muscle tone activity was effective in stabilizing the GHjoint as it made the joint stiffer along all the axes with
reduced difference among the different directions. Further work needs to be done to characterize contributions
of the individual structures (muscles and ligaments) and
the influence of arm positions over a large sample of
specimens, which were limitations of the above study
and should be addressed in further studies.
Acknowledgements
The project was supported in part by Arthrex, Inc.
(LZ), NIH (LZ), and Falk Medical Research Trust. We
would like to thank Maria D. Knoll, PhD, for her
assistance on the statistical analysis.
References
Basmajian, J.V., De Luca, C.J., 1985. Muscle alive: Their functions revealed by electromyography. Williams & Wilkins, Baltimore.
Blasier, R.B., Soslowsky, L.J., Malicky, D.M., Palmer, M.L., 1997.
Posterior glenohumeral subluxation: active and passive stabilization in a biomechanical model. J. Bone Joint Surg. 79-A, 433–
440.
Debski, R.E., Sakone, M., Woo, S.L.-Y., Wong, E.K., Fu, F.H.,
Warner, J.J., 1999a. Contribution of the passive properties of the
rotator cuff to glenohumeral stability during anterior–posterior
loading. J. Shoulder Elbow Surg. 8, 324–329.
Debski, R.E., Wong, E.K., Woo, S.L.-Y., Sakane, M., Fu, F.H.,
Warner, J.P., 1999b. In situ force distribution in the glenohumeral
joint capsule during anterior–posterior loading. J. Orthop. Res. 17,
769–776.
Halder, A.M., Halder, C.G., Zhao, K.D., O’Driscoll, S.W., Morrey,
B.F., An, K.N., 2001a. Dynamic inferior stabilizers of the shoulder
joint. Clin. Biomech. 16, 138–143.
Halder, A.M., Kuhl, S.G., Zobitz, M.E., Larson, D., An, K.N., 2001b.
Effects of the glenoid labrum and glenohumeral abduction on
stability of the shoulder joint through concavity-compression. J.
Bone Joint Surg. Am. 83-A, 1062–1069.
Harryman, D.T.I., Sidles, J.A., Clark, J.M., McQuade, K.J., Gibb,
T.D., Matsen, F.A., 1990. Translation of the humeral head on the
glenoid with passive glenohumeral motion. J. Bone Joint Surg. Am.
72, 1334–1343.
Hawkins, R.J., Bokor, D.J., 1990. In: , Matsen III, F.A. (Ed.), The
Shoulder, vol. 1. W.B. Saunders Co., Philadelphia, pp. 149–
177.
Helmig, P., Sojbjerg, J.O., Sneppen, O., Loehr, J.F., Ostgaard, S.E.,
Suder, P., 1993. Glenohumeral movement patterns after puncture
of the joint capsule: an experimental study. J. Shoulder Elbow
Surg. 2, 209–215.
Kumar, V.P., Balasubramaniam, P., 1985. The role of atmospheric
pressure in stabilizing the shoulder. An experimental study. J. Bone
Joint Surg. Am. 67B, 719–721.
Makhsous, M., 1999. PhD Thesis, Department of Polymetric Materials, Chalmers University of Technology, Gothenburg, Sweden,
ISBN 91-7197-7810-7190.
Makhsous, M., Palmerud, G., Ericson, K., H€
ogfors, C., 1998.
Influence of tonus, elastic stress and submaximality in static
contraction of shoulder muscles. Studia I Monografie AWF we
Wroclawiu 55, 41–48.
Malicky, D.M., Soslowsky, L.J., Kuhn, J.E., Bey, M.J., Mouro, C.M.,
Raz, J.A., Liu, C.A., 2001. Total strain fields of the antero-inferior
shoulder capsule under subluxation: A stereoradiogrammetric
study. J. Biomech. Eng. 123, 425–431.
Matsen III, F.A., Thomas, S.C., Rockwood Jr., C.A., 1990. In: Matsen
III, F.A. (Ed.), The Shoulder, vol. 1. W.B. Saunders Co.,
Philadelphia, pp. 526–560.
McPherson, E.J., Friedman, R.J., An, Y.H., et al., 1997. Anthropometric study of normal glenohumeral relationships. J. Shoulder
Elbow Surg. 6, 105–112.
McQuade, K.J., Shelley, I., Cvitkovic, J., 1999. Patterns of stiffness
during clinical examination of the glenohumeral joint. Clin.
Biomech. 14, 620–627.
Morrey, B.F., An, K.-N., 1990. Biomechanics of the shoulder. In:
Rockwood Jr., C.A., Matsen III, F.A. (Eds.), The Shoulder, vol. 1.
pp. 208–245.
M. Makhsous et al. / Clinical Biomechanics 19 (2004) 107–115
Moseley, H.F., Overgaard, B., 1962. The anterior capsular mechanism
in recurrent anterior dislocation of the shoulder. J. Bone Joint
Surg. Br. 44, 913–927.
Novotny, J.E., Beynnon, B.D., Nichols, C.E., 2000. Modeling the
stability of the human glenohumeral joint during external rotation.
J. Biomech. 33, 345–354.
Soslowsky, L.J., Malicky, D.M., Blasier, R.B., 1997. Active and
passive factors in inferior glenohumeral stabilization: a biomechanical model. J. Shoulder Elbow Surg. 6, 371–379.
Symeonides, P.P., 1972. The significance of the subscapularis muscle in
the pathogenesis of recurrent anterior dislocation of the shoulder.
J. Bone Joint Surg. Br. 54, 476–483.
Ticker, J.B., Warner, J.J.P., 2000. Selective capsular shift technique for
anterior and anterior–inferior glenohumeral instability. Clin.
Sports Med. 19, 1–17.
115
Walsh, E.G., 1992. Muscles, Masses and Motion. The Physiology of
Normality, Hypotonicity, Spasticity and Rigidity. Blackwell Scientific Publications Ltd., New York, Oxford.
Warner, J.P., Deng, X.H., Warren, R.F., Torzilli, P.A., 1992. Static
capsuloligamentous restraints to superior–inferior translation of
the glenohumeral joint. Am. J. Sports Med. 20, 675–685.
Weiser, W.M., Lee, T.Q., MaMaster, W.C., McMahon, P.J., 1999.
Effects of simulated scapular protraction on anterior glenohumeral
stability. Am. J. Sports Med. 27, 801–805.
Zhang, L.-Q., Butler, J.P., Nishida, T., Nuber, G.W., Huang, H.,
Rymer, W.Z., 1998. In vivo determination of the direction of
rotation and moment–angle relationship of individual elbow
muscles. J. Biomech. Eng. 120, 625–633.