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Clinical Biomechanics 20 (2005) 822–833

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An algorithm for estimation of shoulder muscle forces


for clinical use
Philippe Favre *, Ralph Sheikh, Sandro F. Fucentese, Hilaire A.C. Jacob
Laboratory for Orthopaedic Research, Department of Orthopaedics, Balgrist, University of Zurich, Forchstrasse 340, Zurich 8008, Switzerland

Received 21 October 2004; accepted 20 April 2005

Abstract

Background. The shoulder joint represents an indeterminate mechanical system, making it difficult to predict individual muscle
forces required to equilibrate a given arbitrary external force. Although considerable work has been published on this matter, no
model exhibits the adaptability required for the analysis involving different positions of the humerus and for any external load.
An algorithm involving decision-making loops is developed to predict forces exerted by muscles that cross the shoulder joint in
equilibrating a given external force acting in an arbitrary direction, with the humerus in any one of 12 selected positions.
Methods. Muscle lever arms and directions of action collected from a full-size epoxy model of the shoulder joint are used together
with the external force as input. The algorithm selects an appropriate group of muscles and step by step attributes small force incre-
ments to withstand the external moment while aiming at minimising the forces involved. Each muscle force increment is stored after
every loop and eventually summed up. Stability of the glenohumeral joint is the final determining factor.
Findings. Six worked-out examples show interesting features of probable muscular activity. Muscle segmentation is of paramount
importance for spatial control. Although stability can be achieved by increasing the overall rotator cuff activity (co-contraction), this
is rarely necessary.
Interpretation. The strategy of force sharing among the muscles opens up the possibility to examine the outcome of muscle defi-
ciencies and to investigate causes of joint instability as encountered in clinical practice. Further validation of the model is still
needed, but certain clinical observations can be explained.
 2005 Elsevier Ltd. All rights reserved.

Keywords: Shoulder model; Shoulder muscle forces; Muscle recruitment; Glenohumeral stability; Moment arm lengths; Direction of muscular force

1. Introduction 1990). In addition to particular muscles called upon to


equilibrate an external force, shoulder joint stability
It has long since been recognised that stability of the might require additional augmentation by all the mus-
shoulder joint must primarily be effected through mus- cles of the rotator cuff acting together to provide what
cular action because the relevant joint capsule and liga- is now commonly termed Ôconcavity compressionÕ (Lip-
ments are generally lax throughout the greater part of pitt et al., 1993). It therefore becomes important to
glenohumeral rotation, and hence inactive, while the understand the strategy adopted by muscles in balancing
joint surfaces themselves offer but little resistance to dis- a given external force, while preventing dislocation of
location (Jössel, 1880; Perthes, 1906; Gerber, 1992; Lip- the glenohumeral joint. The complexity of the shoulder
pitt et al., 1993; MacMahon et al., 1995; Kronberg et al., joint, with its extensive range of motion and large num-
ber of muscles, calls for close examination of possible
muscular strategies involved, to understand some of
*
Corresponding author. the disorders of this intricate articulation and to treat
E-mail address: pfavre@research.balgrist.ch (P. Favre). these more effectively.

0268-0033/$ - see front matter  2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.clinbiomech.2005.04.007
P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833 823

Analysis of joint mechanics necessitates prediction of which an arbitrary combination of external loading con-
muscular load sharing, and as long as forces within the ditions would apply. We therefore developed an algo-
living muscles, or at least across the joints, have not rithm to predict muscle forces and test joint stability
been directly measured while performing a given task, from data measured off a full-size epoxy model of the
any estimate of muscle force would depend on the bio- thorax, scapula and arm.
mechanical model chosen. Invariably, one is confronted
with the problem of static indeterminacy: there are more
unknown muscle forces than equilibrium equations. 2. Method
Even electromyographic (EMG) recordings fail to pro-
duce reliable force estimates because the relationship be- 2.1. Definitions
tween force and EMG activity is dependent on several
unpredictable variables (Inman et al., 1952; De Luca 2.1.1. The Coordinate system
and Forrest, 1973; MacMahon et al., 1995; Van der A Cartesian coordinate system referenced to the scap-
Helm, 1994). Several investigators, from the second half ula is used to define the line of action of forces, and the
of the 19th century up to recently (Fick, 1850; Fick, resulting turning moments. It is defined as follows, for
1910; Pauwels, 1965; Murray et al., 2000), have used the right shoulder:
the cross-sectional area of a muscle as being indicative
of the proportion of load taken by it in comparison to • The origin is the centre of rotation of the humeral
synergists that assist in performing a common task. head.
Much work has already been done towards estimat- • The X-axis lies in the scapular plane and is directed
ing the shoulder muscle forces. Many optimisation prin- from medial to lateral.
ciples have been employed to compute the load sharing • The Z-axis is directed caudal to cranial.
between the muscles that cross a joint. One of the first • The Y-axis follows the right-hand rule (directed
was that the sum of all attributed muscle forces should anterior).
be a minimum (Seireg and Arvikar, 1975). Optimisation
principles of minimum energy consumption and mini-
mum muscle stress have also been implemented (Hardt, 2.1.2. Motion components, position, and directional signs
1978; Crowninshield and Brand, 1981). Other criteria Each motion is decomposed into its elevation, flexion
that have been used consider a time-dependent function and rotation components relative to the scapula, which
related to muscular stress-endurance (Niemi et al., 1996) for the present purpose is considered to remain in a fixed
or minimisation of muscular energy consumption (met- neutral position. ÔPositive elevationÕ denotes abduction,
abolic cost) during fast goal directed movements (Hap- Ônegative elevationÕ adduction; Ôpositive flexionÕ is ante-
pee and Van der Helm, 1995). rior flexion, Ônegative flexionÕ posterior flexion or exten-
The work published by Karlsson and Peterson (1992); sion; Ôpositive rotationÕ implies medial or internal
Van der Helm (1994); Happee and Van der Helm (1995) rotation, and Ônegative rotationÕ lateral or external rota-
deserve special mention. Laursen et al. developed an tion. This terminology relates to a spherical system (in-
EMG-based model. Others, like Johnson et al. (1996), stead of a Cartesian) centred at the glenohumeral joint,
have contributed morphometric and coordinate data the loci of any point on the humeral axis within its total
that are indispensable for the estimation of muscle range of motion being a globe. With the axis of this
forces about the shoulder joint. A useful biomechanical globe running in a cranio-caudal direction, degrees of
model of the shoulder complex must realistically repre- longitude would be a measure of flexion, while degrees
sent the lines of action of muscles for all three-dimen- of latitude express elevation. Thus, ambiguity of posi-
sional positions of the arm (Otis et al., 1994; Johnson tion that could arise through confusion of sequence with
et al., 1996; Wickham and Brown, 1998), and although Eulerian angles (CodmanÕs paradox) as in a Cartesian
some information on the Cartesian coordinates of sev- system is prevented.
eral muscle insertions about the shoulder joint have be-
come available, those of the two-joint muscles are not 2.1.3. ‘Given’ external moment and ‘virtual’ external
included, and the problem of ‘‘muscle wrapping’’ in moment
many positions of the arm is not readily solved. The given external moment is the moment induced by
Most of the above mentioned computational meth- the given external force or external pure torque. The
ods have unfortunately been tailored to meet special moment is named according to the direction of move-
cases of loading (usually to balance an external moment ment it would initiate; e.g. an abduction moment causes
acting in one principal direction) and therefore do not abduction, etc.
readily lend themselves for application in a clinical envi- The virtual external moment is defined as the differ-
ronment where one wishes to test, for instance, the effect ence (error) between the given external moment and
of a neurological or muscular deficiency on a model in the partially exerted muscle moment, as determined at
824 P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833

any intermediate step of the iteration procedure. It is Table 1


therefore the remaining external moment that the mus- Physiological cross-sectional area (mm2) and maximal force (N) for the
27 muscles segments
cles still have to balance. At the end of the algorithm,
the sum of all iterate muscle moments opposes in direc- Muscle segments PCSA Max force
tion and equals in magnitude the given external moment 1 SSP1 260 182
within the range of the chosen acceptable error. 2 SSP2 260 182
3 SSC1 450 315
4 SSC2 450 315
2.1.4. Protagonists and antagonists 5 SSC3 450 315
Protagonists are those muscles which exert a mo- 6 ISP1 320 224
ment that counteracts a given component of the exter- 7 ISP2 320 224
nal moment; e.g. the supraspinatus muscle would be a 8 ISP3 320 224
9 TMIN1 100 70
protagonist in equilibrating an external adduction (neg- 10 TMIN2 100 70
ative elevation) moment. Antagonists are muscles which 11 DEL1 860 602
exert a moment in the same sense as that of the external 12 DEL2 290 203
moment component. Any muscle having three compo- 13 DEL3 290 203
nents of action can well be a protagonist for one 14 DEL4 290 203
15 DEL5 430 301
external moment component, but an antagonist for 16 DEL6 430 301
another! 17 TRI 680 476
18 COR 250 175
2.1.5. Muscle segments 19 TMAJ 1000 700
The muscles of the shoulder have been segmented to 20 LAT1 290 203
21 LAT2 290 203
allow for differentiated actions. Some were divided into 22 LAT3 290 203
two, others into three parts. This was especially neces- 23 PEC1 460 322
sary in muscles with broad insertions because moment 24 PEC2 460 322
arm length and direction of tendon action vary consid- 25 PEC3 460 322
erably within a given muscle. Moreover, neuromotor 26 BI CL 310 217
27 BI CB 320 224
control strategies differ across the breadth of muscle
and all fibres in a given muscle must not necessarily con- SSP = supraspinatus, where SSP1 is the anterior part and SSP2 the
posterior.
tract simultaneously (Fick and Weber, 1877; Van der SSC = subscapularis, where SSC1 is the most cranial part, SSC3 the
Helm and Veebaas, 1991; Johnson et al., 1996; Wick- most caudal.
ham and Brown, 1998). Table 1 lists the manner in ISP = infraspinatus, where ISP1 is the most cranial part, ISP3 the most
which the muscles were segmented and also gives values caudal.
of the cross-sectional areas that were used. TMIN = teres minor, where TMIN1 is the cranial part, TMIN2 the
caudal.
DEL = deltoideus, where part 1 is the anterior, 2–4 the middle, and 5–6
2.2. Conditions to be fulfilled the posterior parts.
TRI = triceps.
2.2.1. Force boundaries COR = coracobrachialis.
The maximal force (see Table 1) a muscle can develop TMAJ = teres major.
LAT = latissimus dorsi, where LAT1 is the most cranial part and
is limited by several parameters such as its optimum LAT3 the most caudal.
length, the contraction velocity, the fibre type composi- PEC = pectoralis major, where PEC1 is the most cranial part and
tion and especially the physiological cross-sectional area PEC3 the most caudal.
(PCSA) (Fick, 1910; Karlsson and Peterson, 1992). In BICL = biceps caput longum.
this study, an average of the PCSA values found in BICB = biceps caput breve.
Wood et al. (1989), Veeger et al. (1991), and Van der
Helm (1994) has been used mainly to determine the tary virtual external moment (without overshooting)
maximum muscle force that could possibly occur, this so that the error always decreases.
being k* PCSA, in which k is a constant factor of 0.7
MN m2 as suggested by Wood et al. (1989). 2.2.3. Stability
Moreover, since a muscle can only pull, the force it Once all muscle forces have been obtained, the result-
exerts can only be positive or null. ing joint force (joint resultant) is calculated and its spa-
tial direction computed. If the intersection of this vector
2.2.2. Convergence with the glenoid surface does not lie within the glenoid
The convergence of the algorithm is ensured as long boundaries, the articulation will dislocate. In this case,
as the virtual external moment becomes smaller after stability is gained by increasing the general rotator cuff
each iteration loop. The overall internal moment is muscle force (the so-called Ôconcavity compressionÕ).
thereby so controlled as to always oppose the momen- This entails recruiting such muscles that might, in them-
P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833 825

selves, be primarily antagonistic to the goal of counter- labrum) and humerus resulted. This enabled us to deter-
acting the given external moment. Consequently, in such mine lever arm lengths (by the tendon travel method
cases more protagonistic activity and therefore more (Fick and Weber, 1877; Shiino, 1913; Otis et al.,
overall muscular energy would be required. 1994)) and direction of muscle action (by means of
markers on the simulated tendons with the optical Mo-
2.3. Lever arms and muscle direction measurements tion Analysis system) without being confronted with
problems related to deterioration of biological tissues
Basically, to approach the problem of determining with time. The radius of curvature of the humeral head
muscle forces which would equilibrate a given external measured 23 mm. Also, tendons were simulated by
force acting on the humerus in any chosen position, braided cords of thickness that corresponded with the
knowledge of the spatial direction of the muscles that actually measured thickness of the tendons as encoun-
cross the glenohumeral joint and the length of their mo- tered during dissection, thereby ensuring the determined
ment arms in that particular position of the humerus are moment arm lengths of the corresponding muscles ap-
required. Furthermore, because each muscle can possi- proach the physiological values that might be expected
bly give rise to rotation components about three orthog- through Ôwrapping aroundÕ bone protrusions (Fig. 1a
onal axes simultaneously (for instance, it could abduct, and b). For muscles that cross the joint with deep bellies,
posteriorly flex, and medially rotate the humerus at in particular the deltoid, the cord used in the model
the same time), it becomes necessary to describe the cor- would represent the action of muscle fibres closest to
responding moment arm lengths for each of these three the joint. The moment arms obtained for segments
actions, separately. of the deltoid are therefore minimal values and represent
A realistic three-dimensional model of the thorax, the worst possible conditions. The cords used for the
scapula and proximal humerus was built, based on a subscapularis and infraspinatus muscles were of 4 mm
fresh cadaver adult specimen with no known shoulder- diameter, those for the teres major 3 mm diameter, for
related pathology and which showed no disorders of the deltoid, triceps, biceps caput longum and supraspi-
the glenohumeral joint on macroscopic examination. natus 2.5 mm diameter, for coracobrachialis, teres min-
The fresh specimen was freed of all muscles and capsule, or and biceps caput breve 2 mm diameter and for
taking particular care to ensure the labrum and the car- pectoralis major and latissimus dorsi 1.5 mm diameter.
tilaginous joint surfaces remained intact. During dissec- Points of insertion on the humerus were determined by
tion drawings and photographs were made to document inspection during dissection and by the clearly defined
the sites of muscle origin and insertion. Silicone rubber narrow areas of insertion detectable on the epoxy cast-
moulds of the humerus and scapula were made in order ing (Fig. 1b). Points of origin were chosen along the last
to cast epoxy resin replicas of them. In this manner line of contact between muscle and bone, raised above
dimensionally true epoxy models of the scapula (with the bone surface by about 6 mm (see eyelets in

Fig. 1. (a, b) The epoxy shoulder model used to determine muscle lever arms and directions of muscle action.
826 P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833

Table 2 Table 3
The 12 investigated positions of the humerus with respect to the Lever arm in mm, and unit vectors of tendon direction in which muscle
scapula forces act on the humerus for the 27 muscle segments; humerus in 30
Position Elevation () Flexion ()a Rotation ()b elevation in the scapular plane, in neutral rotation
Elevation Flexion Rotation X Y Z
1 30 30 0
2 60 30 0 SSP1 22.27 5.47 5.48 0.98 0.14 0.16
3 80 30 0 SSP2 23.07 0.00 6.25 0.98 0.14 0.16
4 0 0 0 SSC1 5.90 8.98 15.56 0.95 0.30 0.07
5 30 0 0 SSC2 1.77 5.64 21.35 0.93 0.34 0.14
6 60 0 0 SSC3 12.77 1.43 16.40 0.95 0.25 0.21
7 80 0 0 ISP1 14.46 0.00 15.90 0.96 0.03 0.29
8 30 30 0 ISP2 7.47 3.01 19.55 0.94 0.08 0.32
9 60 30 0 ISP3 0.00 3.01 21.47 0.93 0.07 0.35
10 80 30 0 TMIN1 12.87 0.00 17.21 0.91 0.28 0.31
11 30 0 60 TMIN2 13.80 1.45 12.85 0.91 0.28 0.31
12 60 0 60 DEL1 4.85 25.82 0.00 0.50 0.10 0.86
a
Positive values are anterior to the scapular plane, negative values DEL2 22.90 12.84 0.00 0.79 0.12 0.60
posterior. DEL3 29.11 7.13 0.00 0.80 0.07 0.60
b
Negative values denote lateral rotation. DEL4 10.25 26.0 0.00 0.50 0.21 0.84
DEL5 11.00 31.46 0.00 0.60 0.23 0.77
DEL6 28.60 25.88 0.00 0.68 0.12 0.72
Fig. 1a). Broad flat muscles were segmented in 2–3 parts TRI 32.55 11.48 0.00 0.60 0.03 0.80
and the centreline of each segment was regarded as the COR 3.40 28.66 0.00 0.52 0.17 0.84
line of action. Finally, by virtue of the ÔlabrumÕ, the TMAJ 41.55 12.81 0.00 0.92 0.29 0.26
LAT1 28.22 5.73 6.95 0.87 0.18 0.45
humeral head was centred to the extent that no transla- LAT2 52.63 5.73 7.86 0.66 0.02 0.75
tory motion in any direction could be detected while the LAT3 66.51 5.73 5.09 0.42 0.07 0.90
humerus was rotated within the glenoid cavity, thus PEC1 8.69 28.68 6.16 0.76 0.45 0.47
eliminating possible errors from this source when deter- PEC2 17.20 45.81 7.55 0.59 0.75 0.30
mining moment arm lengths. Data were collected for 12 PEC3 34.40 63.00 12.25 0.32 0.89 0.33
BI CL 17.95 17.27 5.70 0.80 0.60 0.02
discrete positions of the humerus with respect to the BI CB 2.85 31.54 0.00 0.51 0.02 0.86
scapula, as shown in Table 2. In each of the 30, 60
and 80 levels of elevation, three positions of flexion (9
positions), and in 0 elevation only one position of flex- finally fulfil several boundary conditions, some of which
ion (humerus in the scapular plane). Because rotation are anatomically and physiologically set.
was maintained in the neutral position in all the afore- The algorithm for shoulder forces estimation (ASFE)
mentioned cases, two additional cases were investigated involves decision-making iteration loops (see Fig. 2). In
to explore at least two positions in the important act of the main loop, an appropriate group of muscles is first
throwing, or pitching, in which lateral rotation of 60 chosen solely depending on the sign (direction) of the
was chosen in 30 and 60 of elevation in the plane of moment components they could possibly exert, for a
the scapula. Changes in position of the scapula relative given position of the humerus. A small arbitrary force
to the thorax have not been taken into consideration is initially attributed to this set of muscles in proportion
for the present purpose but this would only involve to their cross-sectional area. This approximation is nec-
the pectoralis major and latissimus dorsi muscles. The essary to only start the process of iteration, i.e. to express
corresponding values given in the tables can, however, a first set of equations (one for each of the three internal
be readily corrected once the position of the scapula rel- orthogonal moment components) which, after further
ative to the thorax has been defined. One example of the modification through sub-routines to suit specific bound-
muscle lever arms and directions of action can be seen in ary conditions (admission of only positive muscle forces,
Table 3, the remaining cases can be found in the elec- re-arrangement of individual muscle contributions to
tronic version of this article in Tables A–L. meet directional requisites and to minimise magnitude
of forces involved) leads to an iterate that is a better
2.4. The algorithm approximation of the muscle forces required. Also, by
choosing only small increments of muscle force in each
2.4.1. Synopsis of the algorithm loop and, if necessary by even clipping an already esti-
Because each muscle commonly gives rise to turning mated muscle force, it is ensured that at no stage the
moments in all three orthogonal planes simultaneously, muscular moment overshoots the external one. At any
choice of muscles and the magnitude of force demanded intermediate stage, although the given external moment
from each to equilibrate a given external moment be- components are still not balanced, the amount of imbal-
comes an elaborate issue. Solving the problem therefore ance has decreased. By treating the issuing imbalance,
requires a system of arithmetical operations that have to also referred to as ÔerrorÕ as a new set of external moment
P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833 827

lated in magnitude and direction (positive or negative)


External force and
humerus position with reference to the scapular Cartesian system.
(Input)
2.4.4. The main iteration loop
External moment
Suitable muscle segments are selected, equilibrium
Loop calculation equations solved, and forces attributed to these, as
follows:
Muscle recruitment
2.4.4.1. Muscle recruitment. The main criterion for mus-
F(i) is reduced
cle recruitment is the direction of muscle action. How-
Equilibrium equation
for antagonists ever, since each muscle segment generally exerts
moments in all three orthogonal planes simultaneously,
Average forces
selection of essential muscle segments requires grouping
If there exist i into two categories, as follows:
such that F(i) < 0 Force redistribution
If for all i,
F(i) > 0 (A) Muscle segments that can exert a significant
Force limitation moment to oppose the greatest of the three exter-
nal moment components, while totally disregard-
F(i) is reduced Internal moment ing the two lesser ones.
for antagonists calculation (B) Muscle segments that can exert moments which
Condition 2 oppose all three external components
Error calculation simultaneously.
Condition 1

Virtual moment From category A all muscles with a high potential


If Error reaches
= (large moment magnitude) to exert a protagonistic func-
acceptable limit
Error
tion in opposing the greatest component of the external
moment are primarily chosen. Such muscle segments are
Joint resultant chosen when their individual maximum muscle moment
force
in the direction of interest is greater than the average of
If not stable, ground
level activation is all maximum muscle moments in the same direction
Joint stability
introduced / raised multiplied by a threshold factor. If the threshold value
be high, few muscles with high potential would be re-
Solution cruited to counteract the external moment, whereas
low values lead to several muscles of lower potential
Fig. 2. Structure of algorithm. Condition 1: One or two internal
moment components do not oppose the corresponding virtual moment
sharing the task, resulting in finer tuning of the muscular
components. Condition 2: All three internal moment components moment.
oppose the corresponding virtual moment components. Since it would be logical to assume that neuromotor
control strategy is such that muscles are loaded to the
least extent in performing a given task, it follows that
components, called virtual external moment compo- the issuing magnitude of the joint resultant would also
nents, the process described above is repeated until the be as low as possible. Tests have shown that a minimum
issuing error converges to an acceptable level. Each thus joint resultant force issues with a threshold factor be-
determined muscle force is stored after every loop and tween 0.2 and 1.4 and therefore, the optimal threshold
finally summed up to give the final estimate. factor which leads to the lowest value of resultant force
is sought by iteration.
2.4.2. Input To category B belong those muscles that do not exhi-
The input consists of the given external force and the bit a sufficiently large moment potential in the major
humerus position. The external force is defined by its direction, but which nevertheless favour convergence
point of application and directional components within in all three directions simultaneously. This category
the local Cartesian coordinate system. A choice of one has been found crucial to arrive at an acceptable final
of the 12 discrete humerus positions is presently solution by virtue of the larger number of muscles (or
possible. muscle segments) available. Although these have little
moment potential to equilibrate the major virtual exter-
2.4.3. External moment calculation nal moment component they are indispensable for equil-
From the input data, components of the given exter- ibrating the remaining two components of external
nal moment for elevation, flexion and rotation are calcu- moment.
828 P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833

The strategy used to solve the problem is therefore to 2.4.4.3. Force averaging. The three different results for
first focus on the greatest external moment component every muscle segment arrived at above are dealt with
which calls for a choice of muscles that strongly oppose by attributing the average of the three values to the cor-
this in the first place and to then select other muscles responding muscle. This constitutes a compromise that
that will counteract the two remaining moment compo- would not satisfy any of the single given equations but
nents, too. is the best approximation on the whole.
If the three given external moment components be of
the same amplitude, the programme will continuously 2.4.4.4. Force redistribution for prevention of negative
switch its focus from one component to another, ensur- force values and antagonistic action. Negative muscle
ing convergence of all three components alternately. force values that issue from the equations are not real,
although muscle moments can still be positive or nega-
2.4.4.2. Equilibrium equations. To obtain equilibrium a tive. Given a first choice of muscle forces Fi, the muscles
system of three equations, each for moments in one of of category A may introduce undesirable antagonistic
the three orthogonal planes, must be satisfied. For each effects in the other two directions. Indeed, the total mo-
plane we have: ment of all selected muscles will always oppose the
X greatest virtual external moment component. But, if
ðinternal momentsÞ þ ðvirtual external momentÞ ¼ 0 the antagonists exert together a greater moment than
ð1Þ that of the protagonists in at least one of the two
remaining directions, this would also lead to an increase
where of misbalance in the corresponding direction. In the case
X X of such antagonistic action, the solution of the equations
ðinternal momentsÞ ¼ ðF i  leveri Þ ð2Þ may even lead to negative muscle force values. This is
dealt with as follows:
Fi being the force exerted by the muscle segment ÔiÕ
The protagonists must in any case exert a greater
and leveri its lever arm, where i = 1,2,3, . . . , 27. The
moment than that of the antagonists. To do so, an in-
27Fi are the unknowns of the equation.
ner loop is inserted before the equilibrium equations in
To overcome the problem of indeterminacy we first
the next iteration step to redistribute the forces that
make use of the physiological cross-sectional area,
were first selected on the basis of PCSA, giving less
PCSA (Table 1). Assuming that all protagonists would
weight to the antagonists until the moment exerted by
exert force simultaneously in proportion to their PCSA,
the protagonists exceeds that of the antagonists. In this
one muscle ÔuÕ is chosen and all other muscle forces re-
way, solely positive muscle force values are obtained
lated to it. The PCSA values link together all muscle
and overall protagonistic action is ensured in all three
forces, and thus decrease the number of unknowns from
directions.
27 to 1:
Qi ¼ PCSAi =PCSAu ð3Þ 2.4.4.5. Prevention of overshooting. Because only the
where Qi is the quotient between the PCSA of the muscle signs of the muscle moment components are controlled
ÔiÕ and the PCSA of the chosen reference muscle to oppose that of the virtual external moment compo-
P ÔuÕ. nents and no special considerations have been made to
The sum of all internal muscle moments, (Fi * le-
veri), can then be written as: regulate the amplitude of the muscle components, the
X attributed muscle forces during the first few loops can
ðinternal momentsÞ ¼ F u  ½Q1  lever1 þ Q2 reach excessively high values when the virtual external
moment is high and might result in overshooting the gi-
 lever2 þ    þ 1  leveru ven external moment. This can become problematic for
þ    þ Q27  lever27  ð4Þ convergence and also represents a waste of energy by
demanding over-activity from muscles that are less opti-
Inserting Eq. (4) in Eq. (1) and redistributing, one mal. To overcome this problem, all forces are multiplied
equation containing only one single unknown Fu for in each loop with a constant shrinking factor of 0.05 thus
each of the three orthogonal planes is thus obtained. making the incremental steps very small, which leads to
From the hypothesis that all active muscles develop a a smoother iteration process, as shown in Fig. 3.
force proportional to their PCSA, used as a first approx-
imation towards a solution, each muscle force Fi then 2.4.4.6. Force limitation. If the sum of iterative contri-
follows from Eq. (5): butions of any single muscle reaches its maximal force
value, k* PCSA, where k = 0.7 MN m2, the muscle is
F i ¼ Qi  F u ð5Þ
turned off for the rest of the simulation. Other muscles
The above procedure delivers three values of force for that have not reached their limit must take over to resist
each muscle, one for each plane! the virtual external moment.
P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833 829

Without force increment reduction With force increment reduction

Muscle moment amplitude Muscle moment amplitude

External moment

Iteration steps Iteration steps

Fig. 3. Effect of force increment reduction through a Ôshrinking factorÕ to prevent overshooting.

2.4.4.7. Error calculation. At the end of each loop, the The optimisation criterion may therefore be described
overall three orthogonal muscle moment components as the minimisation of muscle forces leading to a stable
have been calculated and the difference between these glenohumeral joint, that is, a joint resultant of minimal
and the corresponding virtual external moment compo- magnitude which acts within the boundaries of the
nents determined. These differences (error1, error2, er- glenoid.
ror3) are an indication of the remaining amount of
imbalance. The total error is quantified by an amplitude
as follows: 3. Worked-out examples
2 2 2 1=2
amplitude ¼ ½ðerror1Þ þ ðerror2Þ þ ðerror3Þ 
Some worked-out examples are now given involving
The closer the muscle and external moments ap- muscular moments of abduction, adduction, posterior
proach each other, the smaller is this amplitude. The flexion and anterior flexion with the humerus elevated
program stops when the amplitude of the error reaches 30 in the scapular plane and in neutral rotation. The
a chosen set value. external moment to be overcome in all these cases is
9 N m, which, in the following examples, would corre-
2.4.5. Resulting force and rotator cuff ground level spond to a 15 N force acting tangentially, at a distance
activation for joint stability of 0.6 m from the centre of the humeral head, i.e. at the
Once the main loop is completed and all final individ- end of an outstretched arm. No weight has been attrib-
ual muscle forces have been determined, the resulting uted to the arm itself. The particular directions of the
joint force is calculated by adding all muscle forces plus external force were chosen to compare the issuing results
the external force and is checked to fall within the gle- with some of the estimates reported in literature. How-
noid boundaries. Minimisation of muscle forces finally ever, a force in any arbitrary direction and spatial posi-
precipitates in a minimisation of the joint resultant tion could have been used.
amplitude. Furthermore, for the same humerus position as de-
The glenohumeral joint will not dislocate as long as scribed above, two cases of pure torque of 9 N m about
the humeral joint reaction force (the resultant) acts with- the humeral axis have been examined, one of medial and
in the boundaries of the glenoid. This can be enforced one of lateral rotation. The results are shown in Fig. 4.
through co-contraction of the rotator cuff muscles (con-
cavity compression) (Van der Helm, 1994; Happee and 3.1. Muscular abduction
Van der Helm, 1995). This superimposed force exerted
simultaneously by all the rotator cuff muscles (supraspi- This corresponds to an external force that gives rise
natus, infraspinatus, subscapularis and teres minor) is to adduction about the glenohumeral joint. The anterior
referred to as the ground level activation and is in some and middle part of the deltoid, especially the latter
cases indispensable for joint stability. If stability is not (DEL3, DEL4), are particularly active, representing
reached at the end of the process described before, about 1/2 of the joint resultant, followed by the biceps
ground level activation is introduced, or raised, and (long head), supraspinatus and infraspinatus. The gleno-
the algorithm restarted. However, a minimal ground humeral resultant force amounts to 450 N.
level activation force is sought in order to minimise
the required muscular energy. In this study, only active 3.2. Muscular adduction
stabilisation is taken into consideration and passive
mechanisms such as adhesion/cohesion, ligamentous The external force tends to abduct the arm. Teres ma-
stabilisation or suction produced under the action of a jor (TMAJ) takes the greater part in load sharing, with
destabilising force, etc. are not taken into account. the triceps, posterior part of the deltoid, latissimus dorsi,
830 P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833

Fig. 4. Forces exerted by the 27 muscle segments for 6 cases of loading with the humerus in 30 elevation in the scapula plane and in neutral rotation.
The inserted field shows the intersection of the resultant with the glenoid, the right side corresponding to the anterior direction and the left side to the
posterior direction.

caudal parts of the pectoralis major and infraspinatus, 3.5. Muscular medial rotation
biceps (short head), coracobrachialis and teres minor
contributing. The magnitude of the resultant amounts An external turning moment of 9 N m was applied to
to 204 N. rotate the humerus in a lateral direction. The main mus-
cle which equilibrates this is the subscapularis (SSC1,
3.3. Muscular posterior flexion SSC2, SSC3) with a force amounting to about 3/4 of
the joint resultant. The middle part of the deltoid
The external force to be balanced acts anteriorly. The (DEL3, DEL4) and the latissimus dorsi assist. The joint
force exerted by the middle portion of the deltoid resultant amounts to 642 N.
(DEL3, DEL4) reaches a very high value, amounting
to about 2/3 of the total muscle force. The other muscles 3.6. Muscular lateral rotation
involved are the teres major, latissimus dorsi, the poster-
ior part of the deltoid, triceps and infraspinatus. The An external turning moment of 9 N m was applied to
joint resultant exhibits a value of 466 N. rotate the humerus in a medial direction. This is equili-
brated mainly by the infraspinatus (ISP2, ISP3) and
3.4. Muscular anterior flexion teres minor. Coracobrachialis, biceps (short head) and
supraspinatus assist to a small extent. The joint resultant
The external force to be balanced acts posteriorly. amounts to 478 N.
The anterior part of the deltoid (DEL1) becomes the
major contributor while the whole pectoralis major,
the middle deltoid segments DEL2 and DEL3, teres 4. Discussion
minor, the cranial part of infraspinatus, supraspinatus,
subscapularis, biceps (short head), and coracobrachialis We have not found any method described in the liter-
assist. In this particular case, the co-activation of the ature which would allow us to readily estimate the forces
rotator cuff had to be raised to 1.6% of each rotator cuff acting across the glenohumeral joint when an arbitrary
muscle maximal force in order to increase Ôconcavity combination of external loading conditions occur.
compressionÕ which was required to prevent dislocation Although we also have not reached the point where this
of the joint. The joint resultant amounts to 316 N. can be accomplished for every possible position that can
P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833 831

be adopted by the humerus in relation to the scapula, we which are conducive to equilibrating the external force
have chosen a total of 12 particular positions often about a spherical joint. Segmentation of muscles in-
encountered in daily life. creases the number of unknown muscle forces, making
The algorithm presented is not a mathematically condition (a) more difficult to fulfil, but on the other
exact method of arriving at a final solution but, like hand this was found to facilitate equilibration of a given
any iterative method, is a search for an acceptable pos- external force by having more selective variables, thus
sibility within given constraints: tensile muscular activ- making (b) simpler to comply with, through allowing
ity, direction of muscle action, maximum attributable for finer regulation. The individual role played by each
muscle force, minimal energy requirements and position muscle segment becomes obvious and this also vividly
of joint resultant with respect to glenoid boundaries. illustrates the necessity to break down muscles, espe-
The ASFE offers the advantage of very short calcula- cially those with broad insertions, into component parts.
tion time, in generally less than 5 min, with a commonly As already observed by Jössel (1880), muscular units,
available PC when run with the well-known and wide- although anatomically designated as one, must not be
spread Matlab software. functionally considered as one single motor unit, but
A major simplification of the model employed is that made up of several, and this is probably how fine control
scapula motion in relation to the thorax has not been ta- of the neuromuscular system indeed functions (Wick-
ken into account, the former remaining in its anatomi- ham and Brown, 1998).
cally neutral position. Therefore, all elevation angles The worked-out examples (Section 3) illustrate the
mentioned in this presentation are referred strictly to possibility of application of this algorithm clearly. A
the scapula. This would certainly affect the estimated ac- comparison of the results obtained for the 6 different
tion of the thoraco-humeral muscles when the humerus loading cases shows immediately which external loads
is elevated beyond about 30 relative to the scapula, but are more difficult to cope with than others. For the same
this was considered acceptable for the present purpose, external load amplitude, but in different directions, the
since only latissimus dorsi and pectoralis major are in- joint resultant can vary between 204 N (muscular adduc-
volved. All other muscles link the humerus to the scap- tion against an external abducting force) and 642 N
ula, so that movement of the latter does not change the (muscular medial rotation against a turning moment in
directions of action of the muscles as defined in the cho- the lateral direction).
sen scapular coordinate system. Direct comparison of the estimates of muscle activity
The factor k = 0.7 MN m2 (Wood et al., 1989) has obtained through the ASFE with those obtained by oth-
been chosen because it lies in the middle of the consider- ers is difficult because of methodological and geometric
able range of 0.4–1 MN m2 (Crowninshield and Brand, differences. Nevertheless, the middle and anterior del-
1981) found in the literature. However, this factor is of toid and supraspinatus muscles, known to be primary
major importance because it limits the maximal external movers in abduction (Kronberg et al., 1990), are shown
force that can be balanced and needs to be more pre- to play a predominant role for this activity in our model,
cisely determined in further studies. too. Incidentally, the biceps (long head) also appears to
For muscles that cross the joint with deep bellies, in play a significant role in stabilising the humeral head, an
particular the deltoid, the cord used in the model would observation shared by Karlsson and Peterson (1992),
represent the action of muscle fibres closest to the joint. Van der Helm (1994) and David et al. (2000). Laursen
The moment arms obtained for segments of the deltoid et al. (1998) and Kronberg et al. (1990) measured
are therefore minimal values and should in fact be re- EMG activity from the infraspinatus during abduction
placed by values greater than those given in the corre- and considered this as a stabilizer.
sponding tables. However, because of the extreme In the case of adduction, others have attributed the
variability in the morphology of these muscle bellies, latissimus dorsi and pectoralis major a leading role in
and want of relevant details with respect to the path ta- this function. Although all these muscles do indeed
ken by the centroids of cross-section in various humeral come into play, we observe a very important role taken
positions, these minimal values (worst conditions) have by teres major, corresponding to the findings of Pearl et
been presently made use of in the algorithm. Further al. (1992), together with high activity on the part of the
work is required to produce more realistic data for del- triceps. The lower magnitude of the joint resultant
toid action. (204 N) in the worked-out example for adduction indi-
Recruitment and dosage of muscular force to balance cates that the external force applied is far below what
a given external force is the goal of the algorithm; how- can be coped with.
ever, two major problems are encountered: (a) there are Posterior flexion surprisingly called upon the middle
more unknown muscle forces than equilibrium equa- part of the deltoid (DEL3 and DEL4) to play a domi-
tions, and (b) each muscle (or muscle segment) most nant role. The middle and the posterior deltoids were de-
often exerts forces in all three orthogonal directions of scribed as prime movers for posterior flexion in the
a chosen Cartesian system simultaneously, not all of EMG study by Kronberg et al. (1990). Actually in our
832 P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833

model, these muscle segments bring a modest contribu- ment arm lengths, direction of muscle action, etc. How-
tion to posterior flexion directly, but they are of major ever, it has been shown that with this algorithm, any
value because of their high abduction component which external force (within reasonable limits of magnitude)
is required to neutralise the adduction moments of all can be considered, leading to an estimation of muscle
other important posterior flexors involved (teres major, forces by searching for a solution in which these are a
latissimus dorsi, DEL5, DEL6, and triceps), as can be minimum, resulting in a joint resultant of lowest possi-
seen in Table 3. ble value.
Anterior flexion also incorporates some interesting Finally, the ASFE has been used to analyse clinical
features: While the anterior part of the deltoid (DEL1) observations of instability with torn or weakened shoul-
plays a leading role, as would be expected (Kronberg der muscles and supports the observations made (article
et al., 1990), and pectoralis major (Pearl et al., 1992), in preparation).
coracobrachialis together with the biceps (Van der
Helm, 1994) are also known to be anterior flexors, the
substantial activity of teres minor has not been de- 5. Conclusion
scribed in this context before. Although teres minor does
not exhibit any flexion potential in this case, it is called A useful algorithm has been devised which is capable
upon to compensate the unwanted medial rotation side- of predicting muscle forces for certain given positions of
effect of the anterior flexors (see Table 3). Interestingly, the humerus in equilibrating an external force acting in
anterior subluxation of the glenohumeral joint in this an arbitrary direction. Good agreement between some
case necessitates an increase of the general rotator cuff worked-out examples using this algorithm and other
activity which, however, entails simultaneous action of simulation studies as well as EMG measurements has
antagonists that increase the magnitude of the joint been found. The strategy of force sharing among the
resultant somewhat. muscles opens up the possibility to reflect on the out-
Medial rotation was seen not to incorporate the ac- come of muscle deficiencies and on causes of joint insta-
tion of pectoralis major, a muscle described as an impor- bility as encountered in clinical practice.
tant medial rotator by Kronberg et al. (1990). This is Further work would aim at examining the influence
because the very high anterior flexion activity of this of scapular rhythm, and the formulation of algebraical
muscle makes it unsuitable. Subscapularis on the other functions that would allow determination of the re-
hand is much more efficient, in combination with latiss- quired anthropometrical data (moment arm lengths
imus dorsi (both cited as prime movers by Kronberg and directions of muscle action) for a general position
et al., 1990) and the middle part of the deltoid. The latter of the humerus within its physiological range of motion,
can, in our study, more easily compensate the unwanted without the necessity to refer to tables containing data
anterior flexion effect of subscapularis. that apply only for discrete positions. Also, additional
Lateral rotation required the action of infraspinatus validation of the model is needed.
and teres minor, as also reported in the literature (Bas-
majian and De Luca, 1985; MacConaill and Basmajian,
1977). In this humerus position, together with the pos- Acknowledgements
terior segment of supraspinatus, they require some com-
pensation from coracobrachialis and the short-head We are most grateful for the unwavering support gi-
biceps to neutralise a posterior flexion tendency. ven by Prof. Christian Gerber M.D., Chairman of the
The good agreement concerning muscle recruitment Orthopaedic Department of Balgrist, University of Zur-
between the results of our study and other simulations ich, during the long course of this project. We also wish
studies as well as EMG measurements show that the to acknowledge the arduous contributions of Dr. Susan-
recruitment criteria described in this study (groups A na Schärli, Mr. Daniele Müller, Dr. Reto Bertani and
and B) lead to meaningful results. Mr. Jordan Velikov, who collaborated with us during
The examples show that in most situations, rotator early phases of this project, and especially the assistance
cuff co-activity is not required for stability. The resultant of Mr. Hans-Rudolf Sommer of the Biomechanics Lab-
mainly falls within the glenoid boundaries without oratory, who made the epoxy models and attended to
necessitating any co-contraction. This also ensures that the measuring equipment.
the magnitude of the resultant is kept as low as possible.
It must again be emphasised that as in any model
which endeavours to predict muscle forces, the solution Appendix A. Supplementary data
arrived at is strongly determined by the given boundary
conditions. In this model we have seen that the amount Supplementary data associated with this article can
of segmentation of each muscle plays an important role, be found, in the online version at doi:10.1016/
apart from the commonly known factors such as mo- j.clinbiomech.2005.04.007.
P. Favre et al. / Clinical Biomechanics 20 (2005) 822–833 833

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