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The effect of muscle fatigue on knee joint proprioception in ballet dancers and non-dancers.

Ballet dancers are frequently characterized as demonstrating excessive knee joint laxity. (1, 2) Proprioception of the knee joint is a topic of interest in dance science and training. (3, 4) Intensive dance training seems to affect motion sense acuity; dancers detect slight changes in knee angles much earlier and more consistently than do non-dancers. (1-5) Contrastingly, tests have shown ballet dancers' position sense acuity to be significantly inferior to that of healthy, active, age-matched controls. (6) Although muscle strength due to intensive ballet training might influence the position or motion sense in dancers, it is not clear how muscle fatigue affects this sense in dancers as compared to non-dancers. (7)

Proprioception is the conscious or unconscious perception of position and motion of an extremity or a joint in space. It includes position and motion sense, detected by mechanoreceptors located in the skin, muscles, and joint tissue. (8) With the replication of a given knee angle (position sense) and the detection of a motion onset (motion sense), the acuity of an individual's proprioception can be measured. It is presumed that the knee joint is stabilized through active neuromuscular control, provided by muscle and proprioceptive stimuli, and by passive restraint, provided by ligaments and capsules. (9) Joint proprioception has an additional role in the neuromuscular control of the knee; therefore, an important influence on movement. During movement, proprioceptive input comes from the knee joint and muscle receptors. According to Hiemstra and coworkers, (9) the greatest contribution to position and motion sense is from muscle receptors, primarily muscle spindles and Golgi tendon organs. Therefore, it could be assumed that muscle fatigue affects position and motion sense. (10)

Muscle fatigue can be defined as the transient inability of a muscle to maintain force during repeated muscle contractions. (10) Muscle fatigue can be achieved and registered in several ways; however, the average peak torque of both knee extension and flexion muscles is frequently used as an indicator of muscle fatigue. (11-15)

As a valuable tool in the study of injury risk factors in dance, it is important to gain insight into how both dancers and non-dancers respond to muscle fatigue. It can be hypothesized that highly trained dancers have well developed sensory acuity and muscle strength, so they can respond appropriately to muscle fatigue. (15) Conversely, those without training (non-dancers) and consequently less muscle strength and proprioceptive acuity are hypothesized to be less capable of reacting properly to muscle fatigue, although they may be capable of adequately detecting their joint positions and motions. (16) Therefore, the aim of this study was to evaluate the influence of muscle fatigue on knee joint position and motion sense in highly trained dancers versus untrained controls.

Methods

Participants

Dancers were recruited from The Hennie Jurrien Foundation in Amsterdam and by word of mouth advertising. The non-dancer control group consisted of students from the faculty of Human Movement Sciences of the VU University Amsterdam, The Netherlands. Inclusion criteria for both groups were: 1. at least 18 years of age; 2. no history of surgery at the hip, knee, or ankle joint of the right limb; 3. no recent (<6 months) musculoskeletal injury of the right leg; 4. no vestibular impairments; and 5. no neurological diseases. A further inclusion criterion for dancers was at least 8 years of ballet training and actively dancing at the time of testing. Participants in the control group were required to have an active lifestyle.

Ten female and three male ballet dancers between 20 and 45 years of age (mean = 27.5 [+ or -] 6.8 years), as well as 9 female and 4 male controls between 23 and 37 years of age (mean = 25.7 [+ or -] 3.7 years) who did not have ballet experience, were included in the study. The dancers had 19.1 [+ or -] 5.4 years of ballet experience. The non-dancers all stated that they exercised in their leisure time. Ten participants among the dancer group and 12 in the control group indicated right leg dominance by answering the question "With which leg would you push off to jump."

The participants were tested at the Amsterdam Rehabilitation Research Center Reade, Amsterdam, The Netherlands. Before participation informed consent was obtained. The study was approved by the local institutional review board.

Procedure

Measurements were performed at the Duyvensz-Nagel Research Laboratory of the Reade rehabilitation center. All participants visited the laboratory once. The right leg was used for all measurements. First, in a non-fatigued state, position sense and motion sense were measured in a counterbalanced order. After these measurements were taken, a 5-minute break was built in, during which participants were asked to walk around as a way of relaxing their muscles. Second, after the break, participants' upper leg muscles were fatigued by maximal isokinetic knee flexion and extension contractions. Third, in the fatigued state, position or motion sense (randomly chosen) was tested, followed by a second 5-minute break. After the second break, the same leg muscles were fatigued again by maximal isokinetic contractions, followed by the last position or motion sense test.

Measurements

Proprioception measurements were performed with an isokinetic dynamometer Biodex System (Biodex Medical Systems, Inc., Shirley, New York, USA). To neutralize cutaneous sensation, inflatable air splints for the lower leg were used (Ferno UK Limited, West Yorkshire, England). Subjects wore blindfolds for both tasks to eliminate vision and headphones with white noise in the motion sense task to eliminate auditory cues.

Participants were seated in the dynamometer chair in an upright position, with the left leg hanging freely over the edge of the chair and the right leg fixed to the attached free-moving arm, with a flexion angle of approximately 90[degrees] (Fig. 1). To perform position and motion sense measurements without any input from active muscle contractions that could influence the participant's perception, both measurements were performed passively.

The initial starting position for both tasks was 90[degrees] of knee flexion.

Position Sense Measurement

The measurement of position sense was based on former studies. (6, 11, 13) A test trial was performed to familiarize the participant with the procedure. After this test trial, six measurement protocols were used. Each protocol included three target angles (30[degrees], 45[degrees], and 60[degrees], respectively) in a random order. (17) Two protocols out of six were randomly assigned to each participant. Each target angle was repeated twice, resulting in six data points per participant in a non-fatigued state and six in a fatigued state.

Before beginning the test, participants were instructed to focus on the leg position. The right leg was then passively moved with a velocity of 4[degrees]/s toward the target angle specified by the protocol. As soon as the attached free-moving arm reached the target angle, it stopped and held this position for 5 seconds. After the leg was released, it was passively extended at a speed of 4[degrees]/s and brought back to the initial starting position. The participant was instructed to push a hold button as soon as he or she sensed that the target position was reached again. Any deviation in degrees from the target position was defined as the absolute position error and used in the analyses.

Motion Sense Measurement

The measurement of motion sense was also performed in accordance with former studies. (18-20) The participants were again familiarized with the procedure during a test trial. After the test trial, two measurement protocols were used. One protocol consisted of starting angles 30[degrees], 45[degrees], 30[degrees], sequentially, while the second consisted of starting angles 45[degrees], 30[degrees], 45[degrees], sequentially. These protocols were assigned to each participant in a counterbalanced order. Each starting angle was repeated twice, resulting in six data points in a non-fatigued state and six in a fatigued state.

The right leg was passively moved into the starting angle specified by the protocol. A touch on the participant's shoulder signaled that at any time within 5 seconds from this signal the lower leg would start to be moved. From this starting angle, the lower leg was passively extended at a velocity of 0.25[degrees]/s. A hand button to stop the movement was pressed as soon as the participant detected knee motion. The deviation in degrees between the starting angle and the detection moment of knee motion was the motion sense error and used in the analyses.

Muscle Fatigue Protocol

The muscle fatigue protocol was based on former studies. (11, 12, 20) While seated in the same testing position, participants actively moved their right leg. Three trials were done beforehand: one flexion and extension movement at a rate of 60[degrees]/s and two at 180[degrees]/s. Five flexion and extension movements were performed to determine the participant's peak torque. For this, the Biodex was set at a rate of 60[degrees]/s to measure isokinetically extension and flexion muscle strength. Subsequently, participants performed 40 isokinetic flexion and extension repetitions at a set maximum rate of 180[degrees]/s. Before the beginning of the protocol, the participants were asked to perform maximal muscle contractions, and the examiner additionally encouraged them verbally to perform the strongest contractions possible. The initial five flexion and extension contractions were then repeated. Comparison of these results with the average peak torques before position and motion sense measurements showed the participant's percentage drop in muscle strength.

Statistical Analysis

A 2x2 mixed factorial repeated measures analysis of variance (ANOVA) was used on the two variables: position sense and motion sense with the factor "group" as between-subject factor (two levels: dancers and controls) and "condition" as within-subject factor (two levels: non-fatigued state and fatigued state). The data were analyzed for main effects of group and condition and for interaction effects between condition and group. The analyses were performed using the SPSS computer software system, version 17.0. Statistical significance was set at p < 0.05. Results were interpreted within a confidence interval of 95%.

Results

All 26 participants successfully completed the tests. The percentage drop in muscle strength of extension and flexion, calculated by comparing the average peak torques before position and motion sense measurements in dancers and controls, is shown in Table 1. The standard deviation for muscle fatigue was high compared to the mean, indicating a large variation in muscle fatigue within both groups. In dancers, the percentage drop in extension and flexion muscle strength for position sense testing was -15.68 (SD 17.00) and -15.56 (13.94), respectively. For motion sense testing the percentage drop of muscle strength was -17.35 (15.48) and -16.47 (16.84), respectively. In controls, the percentage drop in extension and flexion muscle strength for testing position sense and motion sense was -15.48 (11.69), -17.78 (10.36), -15.10 (18.05), and -20.60 (14.90), respectively. These differences were not statistically significant between dancers and controls: extension strength during position sense testing F(1,24) = 0.562, p = 0.562 and flexion strength F(1,25) = 1.899, p = 0.649; extension strength during motion sense testing F (1,24) = 0.044, p = 0.736 and flexion strength F(1,24) = 0.117, p = 0.514, respectively.

Influence of Muscle Fatigue on Position Sense and Motion Sense Position Sense

The influence of muscle fatigue on position sense in degrees in dancers and controls is presented in Table 2. Overall, there was no influence of muscle fatigue on position sense: F(1,24) = 0.239, p= 0.629. There was no difference between dancers and controls (F[1,24] = 0.364, p = 0.552), and no influence of the interaction between group and condition (F[1,24] = 0.412, p = 0.527). In the fatigued state, the dancers showed a lower position sense error than in the non-fatigued state, but the difference was not significant (p = 0.476).

Motion Sense

The influence of muscle fatigue on motion sense in dancers and controls is also presented in Table 2. Muscle fatigue influenced motion sense error significantly (F[1,23] = 6.391, p = 0.019), but there was no significant difference between dancers and controls (F[1,23] = 1.023, p = 0.322). The interaction between group and condition did not influence motion sense: F(1,23) = 2.145, p = 0.157. A higher absolute motion sense error was found in the fatigued state of dancers and controls. The change in motion sense after muscle fatigue was not significant in dancers (p = 0.585) but significant in non-dancers (p = 0.030).

Discussion

In this exploratory study, it was shown that muscle fatigue due to maximal isometric flexion and extension muscle contractions did not affect proprioceptive acuity in highly trained dancers. In non-dancers muscle fatigue by maximal isometric muscle contractions affected motion sense but not position sense. These findings support the hypothesis that long-term ballet training might be an important factor in the capability of ballet dancers to withstand the influence of muscle fatigue on proprioceptive acuity.

Our findings suggest that physical training may also improve the resistance of proprioceptive acuity to muscle fatigue in healthy non-dancers. In only one previous study has this effect been explored. Bouet and Gahery (21) found that acuity and precision of position sense improved significantly after muscle training in otherwise untrained participants. No information on motion sense was available. We believe that our results on both position sense and motion sense are important for increasing knowledge regarding proprioceptive acuity. However, such knowledge with reference to both healthy individuals and those with a musculoskeletal disease is still sparse. Therefore, future studies are needed to replicate and substantiate our estimation of the influence of muscle fatigue due to maximal isokinetic muscle contractions on proprioceptive acuity.

In the current study, proprioception was measured in two ways: knee joint motion sense and knee joint position sense. (9) Several other measurements of proprioception have been described; however, the results of these measurements correlate poorly. (17) It seems that knee joint motion sense and position sense are different aspects of knee proprioception, probably derived from different mechanical receptors. Therefore, both aspects of proprioception were included in the current study. Knee joint position sense might be more representative of real life proprioception, but motion sense seems to be more reliable. (9) A more functional way of testing proprioception is in the standing position. (22) However, weightbearing tests involve more receptors than non-weightbearing tests, so that the result of these tests could be confounded by pain, muscle strength, and balance. (22) It is expected that muscle strength and balance capacity are well trained in dancers, more so than in non-dancers, and could influence the proprioception test. For this reason, the standing test of proprioception was not used. Additional studies are needed on several aspects of the measurement of proprioception.

One reason that muscle fatigue apparently does not affect position and motion sense in dancers might be a strengthened functional link between contractile and sensory muscular processes as a result of many years of physical training. Dance training involves the execution of highly coordinated movements, and even during prolonged training and concomitant fatigue, the proprioceptive system should interact intensively with the muscular system to prevent dancers from sustaining injuries. Some studies have indeed shown that position and motion sense acuity can be increased by the use of specific exercises. (2, 3, 5, 14, 21) However, these studies have only shown that exercise can induce shortterm effects on acuity; therefore, longitudinal studies are needed to explore the long-term effects of these exercise programs.

Even though the proprioception of dancers does not seem to be affected by fatigue, injury incidence rates are high in dancers. (23) Position or motion sense acuity might, therefore, be influenced by other factors than maximal contraction-induced muscle fatigue. For example, laxity of the knee or ankle joint might affect proprioception acuity. Hiemstra and colleagues found increased laxity to be associated with poor proprioception, (10) although other studies did not bear this out. (6, 8, 20) Dancers are characterized by high joint laxity, (1) and an interaction or mediating effect of laxity on the relationship between muscle fatigue and proprioceptive acuity might be expected. Additional studies with the aim of exploring this connection in highly trained individuals such as dancers are needed.

Limitations

The study has some limitations. Firstly, there was a large variation in the degree of fatigue induced by the isokinetic muscle contractions, with fatigue ranging from -48% to -0.2% of the maximal muscle strength. A reason for this could be variability in fatigue resistance but also in different degrees of motivation to perform maximal muscle contractions. The large variability may have obscured some effects of fatigue on proprioception; however, it was similar in dancers and controls, so differences in responses between the groups are not likely affected by this variability.

Secondly, a mul have been preferable (but for practical reasons this was not possible). Repeating the measurements would increase the reliability of the results. A multi-day design might also have reduced learning effects resulting from the fact that the non-fatigued state was always tested first. The differences between groups, however, were probably not (or less) influenced by learning effects because 1. both groups started the tests in the non-fatigued state, and 2. the counterbalanced order of the position sense and motion sense tasks should have offset them.

Thirdly, we reported that the non-dancers had an active lifestyle, which was intended to mean that the young Dutch students from the Faculty of Human Movement Sciences exercised more than once a week. However, we did not measure their real activities. Physical activity can be estimated in different ways, e.g., by questionnaire or by performance testing. (24-26) Future studies should include active lifestyle as a possible confounder of the results.

Finally, our study design was a cross-sectional test re-test protocol, indicating that it lacks applicability to the causal effects of long-term training. As previously suggested, longitudinal studies are needed to unravel the interactions between proprioceptive acuity, muscle fatigue, and the changes affected by training.

Conclusion

Muscle fatigue affects knee joint motion sense in non-dancers but not in dancers. Knee joint position sense is not affected by muscle fatigue in either dancers or non-dancers.

Caption: Figure 1 Set-up for the proprioception measurements and the extension and flexion muscle strength testing.

http://dx.doi.org/10.12678/1089-313X.18.4.143

Acknowledgment

We thank Sara Ergin for her assistance in data collection.

References

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Simone Dieling, M.Sc., MOVE Research Institute Amsterdam, Faculty of Human Movement Sciences, VU University Amsterdam, Amsterdam, The Netherlands. Martin van der Esch, Ph.D., Amsterdam Rehabilitation Research Center, Reade, Amsterdam, The Netherlands. Thomas W. J. Janssen, Ph.D., MOVE Research Institute Amsterdam, Faculty of Human Movement Sciences, VU University Amsterdam, and Amsterdam Rehabilitation Research Center, Reade, Amsterdam, The Netherlands.

Correspondence: Thomas W. J. Janssen, Ph.D., MOVE Research Institute Amsterdam, Faculty of Human Movement Sciences, VU University Amsterdam, Van der Boechorststraat 9, 1081 BT Amsterdam; t.w.j.janssen@vu.nl.

Table 1 Mean Decreases in Extension and Flexion Muscle Strength
by Comparing Average Peak-torque Measurements Before Position
Sense and Motion Sense Measurements in Dancers and Controls

                       Position Sense

            Extension muscle         Flexion muscle
                strength                strength
           (mean [+ or -] SD)      (mean [+ or -] SD)

Dancers   -14.56 [+ or -] 17.00   -15.61 [+ or -] 13.91
Control   -15.49 [+ or -] 11.70   -17.78 [+ or -] 10.36

                        Motion Sense

            Extension muscle         Flexion muscle
                strength                strength
           (mean [+ or -] SD)      (mean [+ or -] SD)

Dancers   -17.35 [+ or -] 15.48   -16.47 [+ or -] 16.84
Control   -15.10 [+ or -] 18.05   -20.60 [+ or -] 14.90

SD = standard deviation.

Table 2 Proprioception Acuity Expressed as Position Sense and Motion
Sense Before and After Muscle Fatigue in Dancers and Controls

                  Position Sense (degrees)

           Pre-fatigue          Post-fatigue
           (mean [+ or -] SD)   (mean [+ or -] SD)

Dancers    5.39 [+ or -] 1.85   4.91 [+ or -] 1.35
Controls   4.75 [+ or -] 1.78   4.89 [+ or -] 1.68

                   Motion Sense (degrees)

           Pre-fatigue          Post-fatigue
           (mean [+ or -] SD)   (mean [+ or -] SD)

Dancers    1.38 [+ or -] 0.52   1.51 [+ or -] 1.06
Controls   1.41 [+ or -] 1.08   2.19 [+ or -] 1.45 *

SD = standard deviation; * p = 0.030.


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Author:Dieling, Simone; van der Esch, Martin; Janssen, Thomas W.J.
Publication:Journal of Dance Medicine & Science
Article Type:Report
Geographic Code:4EUNE
Date:Oct 1, 2014
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