OBJECTIVES: The most prevalent disorders of the shoulder are related to the muscles of rotator cuff. In order to develop a mechanical method for the evaluation of the rotator cuff muscles, we created a database of isometric force generation by the rotator cuff muscles in normal adult population. We hypothesised the existence of variations according to age, gender and dominancy of limb. METHODS: A total of 400 healthy adult volunteers were tested, classified into groups of 50 men and women for each decade of life. Maximal isometric force was measured at standardised positions for supraspinatus, infraspinatus and subscapularis muscles in both shoulders in every person. Torque of the force was calculated and normalised to lean body mass. The profiles of mean torque-time curves for each age and gender group were compared. RESULTS: Our data showed that men gradually gained maximal strength in the fifth decade, and showed decreased strength in the sixth. In women the maximal strength was gained in the fourth decade with gradual decline to the sixth decade of life. The dominant arm was stronger in most of the tested groups. The torque profiles of the rotator cuff muscles in men at all ages were significantly higher than that in women. CONCLUSIONS: We found previously unrecognised variations of rotator cuff muscles' isometric strength according to age, gender and dominancy in a normal population. The presented data may serve as a basis for the future studies for identification of the abnormal patterns of muscle isometric strength in patients with pathology of the rotator cuff muscles. Cite this article: Bone Joint Res 2013;2:214-19.
OBJECTIVES: The most prevalent disorders of the shoulder are related to the muscles of rotator cuff. In order to develop a mechanical method for the evaluation of the rotator cuff muscles, we created a database of isometric force generation by the rotator cuff muscles in normal adult population. We hypothesised the existence of variations according to age, gender and dominancy of limb. METHODS: A total of 400 healthy adult volunteers were tested, classified into groups of 50 men and women for each decade of life. Maximal isometric force was measured at standardised positions for supraspinatus, infraspinatus and subscapularis muscles in both shoulders in every person. Torque of the force was calculated and normalised to lean body mass. The profiles of mean torque-time curves for each age and gender group were compared. RESULTS: Our data showed that men gradually gained maximal strength in the fifth decade, and showed decreased strength in the sixth. In women the maximal strength was gained in the fourth decade with gradual decline to the sixth decade of life. The dominant arm was stronger in most of the tested groups. The torque profiles of the rotator cuff muscles in men at all ages were significantly higher than that in women. CONCLUSIONS: We found previously unrecognised variations of rotator cuff muscles' isometric strength according to age, gender and dominancy in a normal population. The presented data may serve as a basis for the future studies for identification of the abnormal patterns of muscle isometric strength in patients with pathology of the rotator cuff muscles. Cite this article: Bone Joint Res 2013;2:214-19.
We hypothesised the existence of variations of generated force
pattern of rotator cuff muscles according to age, gender and dominancy
of limb in normal adult populationWe found previously unrecognised variations of isometric strength
in rotator cuff muscles according to age, gender and dominancy in
a normal populationIn this study we determined a basis for the future development
of muscle testing for diagnosis of disabilities in rotator cuff
musclesStrength – large number of examined individuals enables meaningful
statistical comparisonsLimitation – the standard testing positions for the individual
muscle evaluation involve some contribution of other shoulder muscles
that have synergistic mode of force generation
Introduction
The most prevalent group of disorders of shoulder is related
to the pathological processes in the muscles of the rotator cuff.[1-4] The intrinsic pathology of these muscles
is usually expressed by pain, weakness and restriction of shoulder
movements. The diagnosis of pathology of the cuff muscles is commonly
based on an initial physical examination, which has limited prediction
values, and can be established with a high precision by more sophisticated
imaging modalities such as ultrasound and MRI. Ideally the ultimate
cost-effective diagnostic tool for this purpose should combine the
simplicity and low cost of the physical examination with the precision
of imaging scans. As the mechanical force generated by these muscles
is easily measurable, the pathology of these muscles might be identified
by assessment of the isometric strengths of these muscles with comparison
with the data in normal population. Unfortunately, comprehensive data
on the generation of isometric force by the rotator cuff muscles
in the normal population, including variations according to gender,
age and dominancy, does not exist. As there are no such reference
data for comparison, the evaluation of rotator cuff pathology by
measurement of the generated force is currently impossible. Several attempts
have been made to determine the normal values of the isometric force
of the rotator cuff muscles,[5-11] but these studies
did not provide full data on a wide spectrum of ages in the large
study groups. Those data are therefore insufficient to develop a
statistically reliable diagnostic tool for evaluation of rotator
cuff pathology by mechanical measurements.In this project we hypothesised that by evaluating the isometric
mechanical force generation by the shoulder rotator cuff muscle
in a large number of healthy adult subjects, we would determine
the essential variability of values reflecting normal adult population,
according to age, gender and dominancy of the tested arm. The resulting
data could then provide a statistically sound database for the future
development of a clinical testing of the rotator cuff muscles.
Materials and Methods
Study group
A total of 400 healthy adult volunteers between the ages of 20
and 60 years were tested. The volunteers were recruited from the
Rambam Medical Center and Faculty of Medicine staff. There were
50 men and 50 women volunteers for each decade within the age range.None of the volunteers had a previous shoulder complaint or injury.
On clinical examination performed by one of the authors (AC), they
were confirmed as having no restriction of shoulder movements (active
or passive), no pain in the shoulder girdle or in the cervical area
and negative provocative tests for subacromial impingement or labral pathology.
All the subjects had a normal observed rhythm of scapulothoracic
movement.Most of the clinically important pathological changes in the
rotator cuff muscles (e.g. tears, partial or full, degeneration,
such in different impingement syndromes, calcific tenditis, etc.)
occur in supraspinatus (SS), infraspinatus (IS) and subscapularis
(SSC) muscles. Accordingly, these structures were evaluated in the
present study.
Assessment of isometric strength
Time curves of the tested muscles in both shoulders in every
person were measured at standardised positions. The dominancy of
the tested limb was recorded. The measurements of the isometric
force were performed by a specialised dynamometer (1200 readings/sec,
resolution 0.04 N; Myometer; Atlantech Medical, Nottingham, United
Kingdom).In general, the rotator cuff muscles act synergistically, but there
are several testing positions when one of these muscles generates
the main force.[12] We
used the following optimal positions for the measurements of various
muscles.
Supraspinatus muscle testing
While in seated position, the tested arm was held in 45° of abduction
and 30° of forward flexion with the dynamometer cuff placed above the
elbow. The elbow was flexed to 90°. The lever arm of abduction force
was measured between the centre of the dynamometer cuff and the
point 3 cm distal to the lateral edge of acromion. This position
represents the centre of rotation of the humeral head.
Subscapularis and infraspinatus
muscle testing
In a supine position, the tested extremity is 30°tilted
forwards and fully adducted. This positioning is chosen in order
to eliminate scapular movements and to evaluate the generated forces
close to the scapular plane. The dynamometer cuff was placed on
the forearm and the forces were produced by the internal and external
rotation of the shoulder. The connection between the dynamometer
cuff and the dynamometer was kept perpendicular to the forearm, in
the opposite direction to the force vector, and therefore the lever
arm in this position is negligible.Each strength measurement was performed for a time period of
five seconds. This period of test was chosen as it is empirically
similarly to the widely accepted Constant’s shoulder assessment
scoring method.[13] Two
measurements were performed for each muscle in five-minute intervals
and the highest results were recorded. Characteristic force-time
curves were produced (Fig. 1). For the further evaluation the values
from the beginning of the generated force rise and in the duration
of four seconds were used in order to eliminate the artifacts of
the initiation and completion of measurements. Therefore the information
was recorded as sequence of measurements lasting four seconds. Each
value was multiplied by the lever arm and expressed as a moment
of torque. The results were normalised to the lean body mass (LBM)
in order to eliminate the effect of the variations in the overall fitness
conditions of the examined subjects. The LBM was calculated according
to the following formulae[14]:Sample profiles of force–time curves
as recorded by a dynamometer.LBM (men) = (1.10×Weight) – 128×(Weight2/(100×Height2))LBM (women) = (1.07×Weight) – 148×(Weight2/(100×Height2))The mean values for each group were recorded and the standard
deviation calculated.This project was approved by the Institutional Ethical Committee.
Statistical analysis
We studied the force–time curves. The corresponding values of
force, according to the equal time intervals, were compared by one-way
analysis of variance (ANOVA) followed by post-hoc Tukey
test (for comparison of pairs of result groups) after a normal distribution
of values was determined by the Kolmogorov–Smirnov test. If not
a normal distribution, one-way ANOVA on ranks with Student’s Newman–Keuls post-hoc test
was used. A p-value < 0.05 was considered to be statistically
significant. The calculations of the statistical comparisons were
performed by SigmaStat software v2 (SPSS Inc., Chicago, Illinois).
Results
The results of the muscle testing in all age groups by gender
are given in Table I and Figures 2 to 4. For all muscles tested,
the profile of generated force was significantly higher in men in
comparison to women (all p < 0.001).Graphs showing the mean maximal
torque values of isometric supraspinatus muscle testing in a) men
and b) women, by dominant (D) and non-dominant (ND) side, normalised
to lean body mass. For both the dominant and non-dominant arms in
men, the profiles of the age groups differed in the following order:
fifth > fourth > third > sixth decade (both p < 0.001). For both
the dominant and non-dominant arms in women, the profiles of the
age groups differed in the following order: fourth > fifth > third and
sixth decades (both p < 0.001).Graphs showing the mean maximal
torque values of isometric infraspinatus muscle testing in a) men
and b) women, by dominant (D) and non-dominant (ND) side, normalised
to lean body mass. For both the dominant and non-dominant arms in
men, the profiles of the age groups differed in the following order:
fifth > fourth > third > sixth decade (both p < 0.001). For the
dominant arm in women, the profiles of the age groups differed in
the following order: fourth > fifth > third and sixth decades (p
< 0.001). For the non-dominant arm in women, the profiles of
the age groups differed in the following order: fourth > fifth and third
> sixth decade (p < 0.001).Graphs showing the mean maximal
torque values of isometric subscapularis muscle testing in a) men
and b) women, by dominant (D) and non-dominant (ND) side, normalised
to lean body mass. For both the dominant and non-dominant arms in
men, the profiles of the age groups differed in the following order:
fifth > fourth > third > sixth decade (both p < 0.001). For the
dominant arm in women, the profiles of the age groups differed in
the following order: fifth and fourth > third > sixth decade (p
< 0.001). For the non-dominant arm in women, the profiles of
the age groups differed in the following order: third and fourth
> fifth > sixth decade (p < 0.001).Results of isometric muscle testing
for all age groups in both genders* p-values for comparison between dominant and
non-dominant resultsIn testing of supraspinatus muscle of the dominant limb in men
we found that a significantly higher profile of the force–time curves
was in men in the fifth decade of life, followed by the individuals of
fourth, third and sixth decades of life (p < 0.001) (Table I,
Fig. 2a). The same tendency is seen in testing the isometric supraspinatus
force-time profiles in the non-dominant upper limbs (p < 0.001,
Fig. 2a).In the group of men in the third decade of life there was no
difference in torque–time curves of supraspinatus muscle testing
between dominant and non-dominant limb (p = 0.06), but in all the
other three groups the dominant upper limb generated significantly
higher isometric force by the supraspinatus muscles (all p <
0.001) (Table I, Fig. 2a).In testing of supraspinatus muscle of the dominant limb in women
we found that a significantly higher profile of the force–time curves
was in the fourth decade of life, followed by the individuals of
the fifth decade (p < 0.001) (Table I, Fig. 2b). The values in
the third and sixth decades of life were similar (p = 0.9), and
both significantly lower compared with the other two age groups (p
< 0.001 for both third- and sixth-decade women in comparison
with fourth- and fifth-decade women) (Table I, Fig. 2b).A similar tendency was seen in testing the isometric supraspinatus
force-time profiles in the non-dominant upper limbs, with significantly
higher values in the fourth and fifth decade of life (p < 0.001)
compared with the third and sixth decades of life, which were similar (p = 0.15)
(Table I, Fig. 2b).In women there was no statistically significant difference between
the dominant and non-dominant limb in third and sixth decades of
life (p = 0.9), but there was a significant difference comparing
the curves of dominant and non- dominant limbs in fourth and fifth
decades of life (p < 0.001) (Table I, Fig. 2b).
Infraspinatus muscle testing
Similarly to supraspinatus, we found testing of infraspinatus
muscle of the dominant limb in men to show a significantly higher
profile of the force–time curves in the fifth decade of life, followed
by the fourth, third and sixth decades (p < 0.001 (Table I, Fig. 3a).Testing of infraspinatus in male non-dominant limbs showed similar
high profiles in the fourth and fifth decades of life (p = 0.15),
which were significantly higher than the third and sixth decades
of life (both p < 0.001) (Table I, Fig. 3a). In all age groups
the dominant upper limb generated significantly higher isometric
force by the infraspinatus muscles (all p < 0.001, Fig. 3a).In the dominant arm in women, we found testing of infraspinatus
to result in a significantly higher force–time curve profile in
the fourth decade of life compared with the other decades (p <
0.001) (Table I, Fig. 3b). There was no significant difference between
the dominant limb curve’s profiles in the groups in third and sixth
decades of life (p = 0.03) (Fig. 3b). In non-dominant female limbs,
the significantly highest profile of the force–time curves was in
the fourth decade of life (p < 0.001) in comparison with and
followed by the individuals in the third and fifth decades (Fig. 3b).
The lowest profile of the force–time curves in women was seen among
individuals belonging to the sixth decade of life (p < 0.001)
in comparison with all other age groups (Table I, Fig. 3b). In all
female age groups above 30 years of age the torque–time curves of
infraspinatus muscles were significantly higher in dominant limbs (p < 0.001).
Those of the third decade of life showed no significant difference
in the profile of the curves of the dominant and non-dominant limbs
(p > 0.05, Fig. 3b).
Subscapularis muscle testing
In testing of the subscapularis muscle of the dominant limb in
men we found that a significantly higher profile of the force–time
curves was in men in fifth decade of life in comparison to and followed
by the individuals of fourth, third and sixth decades in descending
order (p < 0.001) (Table I, Fig. 4a). In male non-dominant limbs,
the profile was highest in those individuals in the fourth and fifth
decades, followed by those of the third and sixth decades (p <
0.001) (Table I, Fig. 4a). In all age groups the dominant arm in
men generated a significantly higher force than the non-dominant
arm (all p < 0.001).In testing the subscapularis muscle of the dominant limb in women
we found a significantly higher profile of the force–time curves
in the fourth and fifth decades of life, followed by the individuals
of third and sixth
decades of life (p < 0.001) (Table I, Fig. 4b). The subscapularis force-time
profiles in the non-dominant upper limbs were highest in the female
individuals in the third and fourth decades of life, followed by
the curves in fifth and sixth decades of life (p < 0.001) (Table
I, Fig. 4b). In all the tested groups of women the dominant upper
limbs generated a significantly higher isometric force by the subscapularis
muscles (p < 0.001) (Table I, Fig. 4b).
Discussion
The use of a portable dynamometer for measurement of isometric
muscle force is known to be precise and efficient.[15] We therefore employed
this method to determine the normal values of isometric force generated
by the rotator cuff muscles. We chose to measure the isometric forces
in positions of the arm that do not provoke subacromial impingement,[12] i.e. in 45° of
abduction and 30° of forward flexion for supraspinatus muscle evaluation, without
reaching 90° of abduction in the scapular plane. In this position
a maximal effort of the supraspinatus is generated, according to
electrophysiological analysis.[7] Also,
secondary discomfort of subacromial irritation as a result of narrowing
of the subacromial space at 90° of shoulder abduction is eliminated.
The latter is of special importance, as in further studies in patients
with subacromial narrowing, a comparison with the present normal values
will be considered.The present data show the expected higher profiles of the torque-time
curves of all the tested rotator cuff muscles in men compared with
women, and in most comparisons of dominant compared with non-dominant
limbs (except supraspinatus muscles in men and women in the third decade
of life, in women in the sixth decade and of infraspinatus muscle
in women in third decade). Additionally, an unexpected finding showed
that men gradually gained maximal strength in all tested muscles (significantly higher torque–time
profiles to the fifth decade of life, before decreasing in the sixth.
In women the maximal strength was
gained in the fourth decade with gradual decline to the sixth decade
of life. In both men and women, in the third decade of life the
generated isometric force of the tested muscles of the rotator cuff
were significantly lower and comparable only to the individuals
in the sixth decade of life, except the values from subscapularis
muscle of non-dominant arm in women (Fig. 4b). The logical explanation to
the drop of the generated isometric force in the sixth decade age
group might be related to development of subtle sub clinical intrinsic
degenerative changes in the rotator cuff muscles in this age group.[3,11] But the reason for the relatively
low profiles of the generated muscle force in third decade of life
is not obvious. Some indication of these unexpected findings can
be found in previous reports[8,16] of small groups
of tested individuals with non-normalised reported data. In the
present study we provide substantial data to show that normal individuals
of both genders in the third decade of life do not reach the maximal
isometric strength in their rotator cuff muscles. The reason for
this phenomenon is not clear but it might have an important impact
on determining goals of physical activities and muscle rehabilitation
in this age group. Further studies are needed to explain the reason
for the observed gradual increase in muscle strength far until the
fourth and fifth decades of life.In this study we determined a basis for the future development
of muscle testing for diagnosis of disabilities in rotator cuff
muscles. The recognition of the normal values of isometric strength
of the rotator cuff muscles will enable identification of the abnormal
patterns of muscle isometric strength in patients with shoulder
rotator cuff pathology in future studies. Recognition of these patterns might
provide a reliable tool for a development of an effective strength
testing method for diagnosis of disorders in the rotator cuff.
Table I
Results of isometric muscle testing
for all age groups in both genders
Mean (sd) maximal torque (Nm/kg)
Muscle/group
Third decade
Fourth decade
Fifth decade
Sixth decade
MEN
Supraspinatus
Dominant
102 (35)
110 (35)
122 (43)
89 (35)
Non-dominant
100 (34)
107 (34)
116 (40)
85 (35)
p-value*
0.06
< 0.001
< 0.001
< 0.001
Infraspinatus
Dominant
51 (13)
55 (11)
57 (20)
45 (16)
Non-dominant
49 (13)
52 (14)
52 (14)
44 (16)
p-value*
< 0.001
< 0.001
< 0.001
< 0.001
Subscapularis
Dominant
102 (35)
110 (35)
122 (43)
89 (35)
Non-dominant
69 (22)
75 (22)
75 (22)
58 (22)
p-value*
< 0.001
< 0.001
< 0.001
< 0.001
WOMEN
Supraspinatus
Dominant
53 (17)
63 (23)
57 (25)
53 (17)
Non-dominant
54 (16)
61 (21)
56 (22)
54 (16)
p-value*
0.15
< 0.001
< 0.001
0.09
Infraspinatus
Dominant
33 (10)
37 (12)
34 (16)
32 (9)
Non-dominant
32 (10)
34 (12)
32 (10)
30 (9)
p-value*
0.9
< 0.001
< 0.001
< 0.001
Subscapularis
Dominant
44 (12)
47 (18)
47 (18)
42 (12)
Non-dominant
43 (13)
43 (13)
41 (22)
40 (10)
p-value*
< 0.001
< 0.001
< 0.001
< 0.001
* p-values for comparison between dominant and
non-dominant results
Authors: H Mike Kim; Sharlene A Teefey; Ari Zelig; Leesa M Galatz; Jay D Keener; Ken Yamaguchi Journal: J Bone Joint Surg Am Date: 2009-02 Impact factor: 5.284