J Sport Rehabil. 2006,15, 312-325
© 2006 Human Kinetics, Inc.
Recovery of Joint Position Sense
in the Shoulder After Muscle Fatigue
Hsiao-Yun Chang, Chen-Sheng Chen, Shun-Hwa Wei,
and Chi-Huang Huang
Context: Fatigue of the shoulder rotator muscles may negatively affect joint position sense (JPS) and ultimately lead to injury. Objective: Recovery of shoulder JPS
after muscle fatigue. Design: A repeated-measures study. Setting: Musculoskeletal
research laboratory. Patients: Thirteen subjects participated in joint position error
tests and isokinetic concentric strength assessment in shoulder rotation, before and
after rotator muscle fatigue. Interventions: Local muscle fatigue was induced using
isokinetic concentric contractions of the shoulder rotator muscles. Main Outcome
Measurements: Shoulder rotator strength and JPS error signals were measured
before fatigue, immediately after fatigue, and every ten minutes thereafter for one
hour. Results: Before shoulder rotation muscle fatigue, the accuracy of shoulder
JPS was 2.79 ± 1.67 degrees. After muscle fatigue, the accuracy decreased to
6.39 ± 2.90 degrees. Shoulder JPS was influenced up to 40 minutes after muscle
fatigue, but shoulder strength was only affected for 10 minutes after muscle fatigue.
Conclusions: Proprioceptive recovery was slower than strength following fatigue
of the shoulder rotators. Key Words: proprioception, muscle fatigue, isokinetic
strength, recovery times, shoulder injuries.
Although the shoulder allows for a high degree of mobility, it is an inherently unstable joint. Thus, balanced control between mobility and stability of the
shoulder joint is required to sustain optimal function. Shoulder stability is based
on a complex interaction between static and dynamic factors. As shown in recent
studies, shoulder proprioceptive receptors may play an important role in maintaining dynamic joint stability.1,2 When shoulder motion reaches its terminal range,
it relies on the early input of proprioceptive information to detect its strain limit
and avoid injury.2-4 Shoulder proprioception is derived from the sense of position
and movement without visual cues,2-5 and two types of mechanical receptors are
responsible for providing the proprioceptive information: (1) the load and tensile
sensitive receptors in muscle spindles and the Golgi tendon organ2-4 and (2) the
stretch-sensitive receptors in the fibrous capsule and ligaments.2-4 Based on studies
Hsiao-Yun Chang is a doctoral student at the Graduate Institute of Physical Education, National College
of Physical Education and Sports, Taoyuan, Taiwan, R.O.C. and is affiliated with the Department of
Physical Therapy, Chung Shan Medical University Hospital, Taichung, Taiwan, R.O.C. Chen-Sheng
Chen and Shun-Hwa Wei (E-mail: [email protected]) are with the Graduate Institute of Rehabilitation Science and Technology, National Yang Ming University, Taipei, Taiwan, R.O.C. Chi-Huang
Huang is with the Graduate Institute of Athletic Training, National College of Physical Education and
Sports, Taoyuan, Taiwan, R.O.C.
312
Recovery of Shoulder JPS
313
involving human cadavers, several investigators have demonstrated that numerous nerve endings spread within the glenohumeral capsule and free nerve endings
are located in the glenoid labrum.1,6 These neural structures are likely to provide
important input on joint position and strain.
Articular cartilages do not contain neural elements, hence articular cartilages
play only a minor role in the sense of joint position and movement of the shoulder
joint. In contrast, the muscles around the shoulder joint are likely to provide more
influence on joint stability and movement control, especially during mid-range
motion, as this is when it is thought there is less proprioceptive feedback since
capsule and ligaments are not taut during depolarization of mechanoreceptors.6
Accordingly, Gandevia and McCloskey7 reported that anesthesia to the interrossous
muscle in the metacarpapphalangeal joint and interphalangeal joint of the finger
results in diminished position sense. Indeed, this study clearly demonstrated the
integral role of the muscle spindle and Golgi tendon organ in providing feedback
and dynamic restraint.7
Muscle fatigue is defined as the transient inability to maintain power output or
force during repeated muscle contractions.8-11 Fatigue can occur anywhere along the
pathway of proprioceptive input, or during cortical integration, motor excitatory
drive to the lower motor neuron and neuromuscular junction, and power output
of the muscle.8-10 Previous studies have shown altered input from the shoulder
proprioceptors after shoulder muscle fatigue,5,12-15 indicating decreased acuity of
proprioception after muscle fatigue. However, there is no evidence pertaining to
the time acuity of the proprioceptors recovers following muscle fatigue and if
proprioceptive acuity follows recovery of muscle strength. Therefore, the current
study had two objectives: (1) investigate the influence of muscle fatigue between
shoulder joint position sense (JPS) and strength of shoulder rotators and (2) investigate the relationship between recovery of the strength of shoulder rotators and
shoulder JPS after muscle fatigue.
Methods
Subjects
Thirteen subjects, eight females and five males, voluntarily participated in this
study. The mean age was 24.46 ± 2.07 years, the mean body weight was 65.38 ±
16.62 kg, and the mean body height was 168.5 ± 9.92 cm. All subjects were asked
to perform the test using their dominant arms. The dominant arm was defined as
the arm the subject normally used to throw a ball. All subjects were free of current
injuries and reported no pain, tenderness, or any episodes of instability during the
six months prior to testing. Subjects were further excluded is they had any history
of shoulder surgery. Informed consent was obtained from all participants before
the initiation of the study.
Instrumentation and Device
A Kin Com 125 AP Isokinetic dynamometer (Kin-Com 125AP, Chattanooga Group,
Inc., Hixson, TN, USA) was used in this study. In order to measure joint position
errors during the test, two signals were simultaneously collected: (1) the shoulder
joint position signal and (2) the subject sense trigger signal. Those two signals were
314
Chang et al
Figure 1—The experimental configuration.
used to identify the actual position and the subjectʼs sensed position. All signals
were simultaneously transferred to a computer through a 16-bit analog-to-digital
converter (Biopac Inc., CA, USA). Data acquisition and processing utilized the
Acknowledge V 2.5 software program (Biopac Inc, CA, USA). All signals were
collected simultaneously with a sampling rate of 100 Hz. A schematic diagram is
shown in Figure 1 that depicts the experimental configuration.
Testing Position and Speed
The present study used the scapular plane as a reference for testing shoulder internal
and external rotation. In the scapular plane, the inferior part of the capsule of the
scapulohumeral joint is not twisted as it would be in either the frontal or sagittal
planes, and the humerus is in neutral rotation. To achieve scapular plane movement
during internal and external rotation of the shoulder, each subjectʼs shoulder was
positioned in 45° abduction and at 30° anterior to the frontal plane (Figure 1). The
elbow was flexed to 90° with the forearm and wrist in the neutral position. The
dynamometer head assembly was tilted 45° from the vertical so that the long axis
of the arm was aligned with the rotation axis of the dynamometer. External rotation
was completed from 40° internal rotation to 60° external rotation; internal rotation
was completed from 60° external rotation to 40° internal rotation.
Many studies have measured JPS in the shoulder, but protocols still lack
consistency in testing speed. Speeds previously used have ranged between 0.5 to
10 degrees/sec.37-40 Based on this, in the present study we selected 3 degrees/sec
as the speed of JPS measurement.
For JPS measurement, the dynamometer passively moved each subjectʼs
dominant arm at a speed of 3 degrees/sec. For shoulder strength measurement,
each subject was asked to perform a maximum of 5-repetition concentric shoulder
internal and external rotations at a speed of 90 degrees/sec.
Recovery of Shoulder JPS
315
Experimental Protocols
The experimental protocols in this study included six steps as follows:
Step One: Screening Examination.
During the screening examination, each
subject was asked for an injury history and underwent a physical examination by a
senior sports physical therapist. The subjects were required to satisfy the inclusion
criteria; the subjects were excluded if they had a positive response to any of the
following tests: the shoulder impingement test, the empty can test, the shoulder
apprehensive and relocation test, and the joint laxity test.
Step Two: Subject Positioning and Preparation.
Before data collection, each
subject was positioned in the dynamometer seat and stabilized with a belt (Figure
1). In order to avoid visual and sound interference with shoulder proprioception,
each subjectʼs eyes were covered by a mask and earphones were worn with music
playing. At this point, the dominant armʼs shoulder JPS signals were ready to be
measured.
Step Three: Warm-Up Practice.
Each subject was asked to practice active and
passive modes of shoulder internal and external rotation until the subject was
familiar with the experimental procedure, at which point formal data collection
was begun.
Step Four: Shoulder Pre-Fatigue Strength and JPS Measurement.
In this
step, each subjectʼs maximal shoulder internal concentric strength was measured
at a velocity of 90°/sec with five repetitions. The JPS signals for each subject were
also measured in two steps. An investigator guided the subject to the joint test position, including initial, middle, and terminal joint angular position. Those angles
of each subject were calculated from the full range of shoulder internal/external
rotation motion as the reference angle (Strue). The initial angle was at 5° from full
internal rotation of the tested shoulder. The middle angle was at the mid-point
of full range of motion for shoulder internal and external rotation. The terminal
angle was at 5° from full external rotation of the tested shoulder. An investigator
used a computerized control system of the Kin Com to guide the mechanical arm
of the dynamometer from internal to external rotation of the shoulder to the test
position and then asked the subjects to visualize and sense the test position for
10 seconds. When a subject thought he/she could memorize the test position, the
mechanical arm of the Kin-Com dynamonometer was returned to the position of
internal rotation of the shoulder and the test was begun. The mechanical arm of
the Kin-Com dynamonometer moved passively to the reference angle of internal
rotation to external rotation of the shoulder at an angular velocity of 3°/sec; when
subjects felt that the mechanical arm had reached the reference angle, they pressed
the trigger switch. The angle that subjects felt was designated as Ssense. The first
measurement was defined as T0.
Step Five: Shoulder Internal and External Fatigue Exercise. In this step, each
subject was asked to perform maximal concentric shoulder internal and external
rotation exercises through a full range of motion at a speed of 90 degrees/sec. The
shoulder rotation muscle fatigue was defined as the force output dropped below
50% of its initial value for three consecutive repetitions.17 When a subjectʼs shoulder
fatigue occurred, the experiment proceeded to the next step.
Chang et al
316
Step Six: Shoulder JPS Measurement After Shoulder Fatigue.
In this step,
shoulder rotator strength and JPS signals were measured at specific times: T1,
immediate-fatigue time; T2, 10 min after shoulder fatigue; T3, 20 min after shoulder
fatigue; T, 30 min after shoulder fatigue; T5, 40 min after shoulder fatigue; T6, 50
min after shoulder fatigue; and T7, 60 min after shoulder fatigue.
Data and Statistical Analysis
The root-mean-square (rms) error of JPS was used as to evaluate proprioceptive
function. The smaller error of RMS was mean more accuracy of JPS. The rootmean-square error was defined as
where,
Ssense is the joint position signal measured by the subjectʼs sense trigger,
Strue is true joint position signal transferred by position transducer,
i is from 1 to 6 because six joint positions were measured in one rotation
cycle, and j is from 1 to 3 because three joint rotation cycles were measured
in each tested subject.
A repeated measures ANOVA was used to compare the shoulder strength and
JPS across the measurement times. Scheffeʼs multiple comparisons were used to
test different measured timings. Simple regression was used to understand the
JPS recovery associated with different post-fatigue timings. Each null hypothesis
was rejected at an overall significance level less than or equal to 0.05. Statistical procedures were carried out using the SPSS for Windows, V9.0 (SPSS, Inc.,
Chicago, IL, USA).
Results
Shoulder rotation strength was measured a total of eight times (i.e., before fatigue,
immediately after fatigue, and in 10-min increments following fatigue for one
hour).
Compared with pre-fatigue strength (T0), post-fatigue strength (T1) decreased
significantly by 39.75% (Tables 1-3), indicating that the tested subjects performed
shoulder internal rotation maximally and did in fact reach fatigue status. The
shoulder rotation strength was found to return to its pre-fatigue level by the 10min post-fatigue measurement (Table 2). Following local muscle fatigue, we thus
demonstrated that strength was rapidly restored, but can also be maintained at the
pre-fatigue level for at least 60 min (Figure 2).
13
13
13
13
13
13
13
13
T0
T1
T2
T3
T4
T5
T6
T7
100.00
39.75
100.21
99.40
103.50
105.59
102.80
106.18
Mean
(%)
0.00
9.98
17.48
14.67
12.72
14.27
9.75
9.79
SD
0.00
2.77
4.85
4.06
3.53
3.96
2.70
2.71
Std. Error
2.7903
6.3871
5.5107
4.3822
4.6497
3.4861
3.6102
2.9250
Mean
(degree)
1.6723
2.8972
2.4305
2.4196
2.6927
2.2510
2.3634
1.9371
SD
Joint Position Sense Error
.3280
.5682
.4767
.4745
.5281
.4415
.4824
.3954
Std. Error
* The times of measurement were T1: immediate-fatigue time, T2: 10 min after shoulder fatigue, T3: 20 min after shoulder fatigue, T4: 30 min after shoulder fatigue,
T5: 40 min after shoulder fatigue, T6: 50 min after shoulder fatigue, and T7: 60 min after shoulder fatigue.
N
Shoulder Rotation Strength
Shoulder Rotation Strength and Joint Position Sense Error at Different Times of Measurement
Time*
Table 1
Recovery of Shoulder JPS
317
318
Chang et al
Table 2 ANOVA Results of Shoulder Rotator Strength and Joint
Position Sense Error
Sum of
squares
Shoulder
rotator
strength
Joint
position
sense error
df
Mean of
squares
F
P
44.059
.000
7.333
.000
Between groups
45416.938
7
6488.134
Within groups
14136.872
96
147.259
Total
59553.809
103
287.165
7
41.024
Within groups
1096.528
196
5.595
Total
1383.688
203
Between groups
Each subject underwent the JPS Errors Test eight times (i.e., before and after
muscle fatigue, as well as every 10 min for one hour after muscle fatigue occurred).
Based on Scheffeʼs multiple comparisons, the JPS errors at T0, T1, and T2 were
significantly different from other measurement times (Table 4; P < 0.05). JPS at
T1, and T2 produced the largest errors. As compared to the recovery of strength, the
restoration of Joint Position Errors was clearly slower. Consequently, we applied
a simple regression line to delineate the relationship between JPS and restoration
time. Figure 2 shows the regression relationships with JPS at post-fatigue times
of 0, 10, 20, 30, 40, 50, and 60 min. As seen in Figure 2, the regression line is
described by the equation, y = 6.93 - 0.07x (r2 = 0.89, P < 0.05). Although the
results of Scheffeʼs multiple comparisons showed that only the JPS errors at T0,
T1, and T2 were significantly different with other post-fatigue times, the regression
line revealed a significant trend (r2 = 0.89, P < 0.05). Therefore, the regression line
uncovered an association between recovery time and JPS error. Furthermore, the
regression line showed that return of JPS errors to the pre-fatigue level required
approximately 40 min.
Discussion
The primary questions addressed in the present study were (1) whether or not
exercise-induced shoulder rotator muscle fatigue increased JPS error and (2) if
different recovery times occurred with respect to muscle strength and JPS. Study
results revealed that shoulder rotator muscle fatigue resulted in a 4o increase in
passive JPS error; however, shoulder rotator strength recovered within 10 min.
Taken together, this suggests proprioceptive accuracy is restored more slowly than
shoulder rotator strength.
Our results demonstrated that muscle fatigue altered proprioceptive acuity, in
agreement with numerous previous studies.5,12,14-15,17-22 Although those studies found
that exercise-induced muscular fatigue affected neuromuscular control deficits,
few studies have investigated recovery of neuromuscular control.23 In the present
Recovery of Shoulder JPS
319
Figure 2—The relationship of shoulder rotator muscle strength recovery, joint position
sense errors, and measurement time.
–5.59
–2.80
–6.18
T6
T7
–3.50
0.59
–0.21
T5
T4
T3
T2
0
60.24*
T0
T1
–66.42*
–63.05*
–65.84*
–63.75*
–59.65*
–60.46*
0
T1
–5.96
–2.58
–5.37
–3.29
0.81
0
T2
–6.77
–3.40
–6.19
–4.10
0
T3
–2.67
0.70
–2.08
0
T4
–0.58
2.79
0
T5
–3.37
0
T6
0
T7
* The mean difference is significant at the .05 level. The times of measurement were T1: immediate–fatigue time, T2: 10 min after shoulder fatigue, T3: 20 min after
shoulder fatigue, T4: 30 min after shoulder fatigue, T5: 40 min after shoulder fatigue, T6: 50 min after shoulder fatigue, and T7: 60 min after shoulder fatigue.
E
M
I
T
(J)
T0
(I) TIME
Scheff’s Post Hoc Multiple Comparison Results of Shoulder Internal Rotator Strength
Mean
Difference
(I)–(J)
Table 3
320
Chang et al
T0
T1
T2
T3
T4
T5
T6
T7
0
–3.59*
–2.72*
–1.59
–1.85
–0.69
–0.81
0.13
0
0.87
2.09
1.73
2.90*
2.77*
3.46*
T1
0
1.12
0.86
2.02
1.90
2.58*
T2
0
–0.26
0.89
0.77
1.45
T3
0
1.16
1.03
1.72
T4
0
1.03
1.72
T5
0
0.68
T6
0
T7
*The mean difference is significant at the .05 level. The times of measurement were T1: immediate–fatigue time, T2: 10 min after shoulder fatigue, T3: 20 min after
shoulder fatigue, T4: 30 min after shoulder fatigue, T5: 40 min after shoulder fatigue, T6: 50 min after shoulder fatigue, and T7: 60 min after shoulder fatigue.
E
M
I
T
(I)
T0
(J) TIME
Scheffe’s Post Hoc Multiple Comparison Results of Joint Position Sense
Mean
Difference
(I)–(J)
Table 4
Recovery of Shoulder JPS
321
322
Chang et al
study, it was shown that recovery of muscle strength was much quicker than JPS.
Similarly, Satxon et al23 also reported that acuity of JPS and muscle tension sense
at the elbow were significantly decreased until five days after eccentric exercise.23
Collectively, these findings suggest that muscle strength and JPS may have different neuromuscular control mechanisms regulating recovery.
Alternatively, the shorter time needed for recovery of muscle strength may
be a reflection of our studyʼs fatigue protocol. The current study used continuous maximal contractions to induce shoulder rotator muscle fatigue. This type of
exercise-induced fatigue causes energy in the muscle tissue to be rapidly depleted.
Thus, there may have been an insufficient supply of bioenergy for muscle fibers to
subsequently execute movements.16 However, after a few minutes of rest, biochemical metabolism restored bioenergy reserves. Hence, this type of exercise-induced
fatigue rapidly led to muscle fatigue yet permitted rapid recovery to prefatigue
levels. Recovery of JPS did not follow a similar mechanism.
According to previous studies, there are two possible explanations that an
exact mechanism for recovery of JPS has not yet been elucidated. First, metabolic
products accumulate after exercise-induced muscle fatigue. Several biochemical
moieties, such as bradykinin, arachidonic acid, prostaglandin E2, potassium, and
lactic acid are produced or released.24-32 All these biochemical products affect the
firing of group III and IV muscle afferents. The resulting aberrant firing patterns,
in turn, result in changes in muscle tension and decreased receptor sensitivity for
the detection of muscle length changes.24-32 Because removal or dilution of these
biochemical moieties requires time, their persistence in the tissues renders proprioceptors less sensitive than at the prefatigue level. Second, muscle fatigue may
affect the sensitivity of muscle mechanical receptors. Several studies have revealed
that muscle fatigue results in decreased neural excitation levels in muscle spindles
and the Golgi tendon organ.33-36 Macefield et al34 investigated ankle dorsiflexors
maintained in an isometric contraction for one minute, finding that the firing rate
for the muscle spindle decreased 72% and significantly decreased its sensitivity.34
Hutton and Nelson35 assessed the Golgi tendon organ in a catʼs gastrocnemius
muscle after exercise-induced fatigue, finding that Ib receptors appeared to be in a
post-excitation depression.35 Altogether, these findings suggest that JPS may also
be affected because muscle mechanical receptors cannot send acuity signals for
distinguishing muscle length and tension during shoulder joint motion. Unfortunately, these previous studies did not provide a consensus to explain the reason
why proprioception requires more time in its functional recovery. Nevertheless,
the present study results may prove helpful in establishing recommended rest times
after muscle fatigue so as to prevent shoulder injuries.
Several major findings in the present study may have implications on the prevention of shoulder sports injuries. Mechanical receptors located in the capsular
ligaments of the shoulder were found to be important for detecting joint position.
Acuity JPS was thought to be very important when shoulder motion reached its
terminal range of motion, especially in the direction of external rotation. Many
studies have indicated that excessive stress on the anterior capsuloligaments
may result in proprioceptive deficits, mechanical instability, and neuromuscular
alterations.5,11,17,19,40-41 All these deficits may cause dynamic restraints for impaired
or repetitive injury.4,11,13,19,41 Therefore, clinicians must be aware that recovery of
shoulder JPS may require more time than that of muscular strength. Specifically,
Recovery of Shoulder JPS
323
forty minutes may be a conservative period of time for full recovery of acuity in
shoulder JPS.
In the present study, the selection of 3 degrees/sec for testing JPS movement
may have limitations. In order to eliminate neural reflexive effects from muscle
spindle organs,37-40 slower testing speed leads to higher accuracy in JPS measurement. However, because our study measured JPS reaction for 60 min after muscle
fatigue, this requirement increased the challenges in experimental efficiency and
the accuracy of data collection. Based on this consideration, we decided to use 3
degrees/sec as the testing speed. In order to obtain more convincing data, future
studies related to this issue may consider setting a slower speed to better understand
JPS sensitivity.
Acknowledgment
We acknowledge with appreciation a grant from the Ministry of Education, Aim for
the Top University Plan, Taiwan.
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