Effect of lower extremity

muscular fatigue on motor

control performance
JOHNSTON, RICHARD B. III;
HOWARD, MARK E.; CAWLEY,
PATRICK W.; LOSSE, GARY M.
Medicine & Science in Sports & Exercise . 30(12):1703-1707, Decem-
ber 1998.

Author Information

The Hughston Clinic, P.C., Columbus and Atlanta, GA; OASIS Sports
Medicine, San Diego, CA; and Smith-Nephew Don Joy Research Lab-
oratory, Carlsbad, CA

Submitted for publication December 1996.

Accepted for publication June 1997.

The authors acknowledge Troy Conklin, ATC, Laurie Jenkins, ATC,

and OASIS staff for their technical assistance.
 3/21

Current addresses: M. E. Howard, OASIS Sports Medicine, San Diego,

CA; G. M. Losse, OASIS Sports Medicine, San Diego, CA; and P. W.
Cawley, Smith-Nephew Don Joy Research Laboratory, Carlsbad, CA.

Address for correspondence: Richard B. Johnston, III, M.D., The

Hughston Clinic, P.C., P.O. Box 9517, Columbus, GA 31908-9517.

Abstract

Effect of lower extremity muscular fatigue on motor control perform-

ance. Med. Sci. Sports Exerc., Vol. 30, No. 12, pp. 1703-1707, 1998.

Purpose: The purpose of this study was to determine whether lower

extremity fatigue affects the ability of an individual to balance on an
unstable platform.

Cited Here... Twenty healthy subjects (average age, 29 yr, range, 20 to

39 yr) were tested on an instrumented balance assessment system.
Static tests were done on the limbs unilaterally and then bilaterally,
and finally a dynamic test was performed in which the subject moved
the platform in a circular manner to chase a moving object on a com-
puter screen. After testing, subjects were fatigued using an isokinetic
dynamometer, which imposes closed kinetic chain antagonistic exer-
cise on the ankle, knee, and hip, similar to a stair stepper. No rest was
allowed, and subjects were fatigued to less than 50% of their initial
tested force. Subjects were then immediately retested on the unstable
platform using the same testing protocol. All subjects completed the
testing.

Cited Here... Analysis of pre- and post-fatigue balance results demon-

strated significant decreases in motor control performance on the
 4/21

three static tests following exercise to fatigue in all subjects (P <

0.001).

Conclusions: Our findings support anecdotal evidence that fatigued

individuals are at increased risk of injury because of loss of balance.
Avoidance of fatigue and preconditioning may prevent injury.

Motor control of an extremity is dependent upon visual, vestibular,

and proprioceptive feedback and the reflexive and voluntary muscle
responses. The importance of proprioception in knee function, stabil-
ity, and injury prevention has been studied extensively
(4,6,8,10,11,17,19,20,27,30), particularly with regard to the anterior
cruciate ligament (ACL)-deficient knee (7,14-16,18,22,26,32). Most of
the static and dynamic supporting structures of the knee have proprio-
ceptive roles in knee function. Mechanoreceptors are found in the ten-
dons and muscles surrounding the joint, the cruciate and collateral lig-
aments, the menisci, and the joint capsule (1-3,17-19,25,27-29). A syn-
ergism between the static stabilizers of the knee and thigh muscle ac-
tion in maintaining knee joint stability has been suggested
(4,5,13,21,22,25,32). It is believed that muscle function around the
knee plays a role in stability and injury prevention
(4,5,7,13,20,21,25,26,28).

Theoretically, fatigue should certainly have an effect on this system of

neuromuscular control around the knee. In the neuromuscular loop,
whether in the afferent or efferent direction or both, motor control
would be inhibited by fatigue. While mostly anecdotal, the observa-
tions that ACL ruptures tend to occur most frequently at the end of a
sporting event, when a participant is fatigued, support this reasoning.
This phenomenon has been noted particularly in recreational skiing,
in which ACL ruptures frequently occur at the end of the day (12).
 5/21

Our hypothesis was that lower extremity fatigue does have an effect on
motor control and thus on performance in balancing. The purpose of
this study was to determine whether lower extremity fatigue affects an
individual's motor control performance on an instrumented balance
assessment system.

Back to Top

MATERIALS AND METHODS

Twenty healthy subjects were used for the study: 12 men and 8 wo-
men, with an average age of 29 yr (range, 20 to 39 yr). None of the
subjects had a recent or remote history of significant lower extremity
injury, and none had a history of lower extremity or spinal surgery. No
subject had a history of vestibular or central nervous system balancing
problems. All the subjects could be considered recreational athletes.
Most (16/20) participated in some form of physical activity at least
three times per week. None were collegiate or professional athletes.

Motor control performance was determined by an instrumented bal-

ance assessment system (KAT, Breg Inc., San Marcos, CA), which is
commercially available for testing or training balance. The use of this
device and reproducibility of the balance data has been described pre-
viously (23,24). The balance system consists of a circular platform
supported at its central point on a pivot. The stability of the platform
is controlled by varying the pressure in a pneumatic bladder that rests
between the platform and the base of the unit (Fig. 1). A score is calcu-
lated by measuring the distance from the tilted position to the refer-
ence position and adding up the absolute numbers over the duration
of the test (23). Hence, the balancing index is inversely proportional to
 6/21

balancing skill. The lower the score, the better the balance index; zero
is a perfect score.
7/21
 8/21

Figure 1-Subject on balancing device (KAT, Breg, Inc., San Marcos,

CA). A) Schematic diagram; B) Photograph.

The subjects performed the tests barefoot with knees slightly bent and
arms folded across the chest and looking forward. They were instruc-
ted to keep the platform as level as possible. Each subject was given a
1-min practice period to become familiar with the balance device (23).

The subjects' balance skills were assessed using four different balance
tests before and after exercising to fatigue. A unilateral static test was
done with each lower limb. In this test the foot of the side being tested
is planted in the center of the platform. A bilateral static test was per-
formed next. The final test was a dynamic balance study in which the
subject, with the feet planted on the platform 10 inches apart, must
move the platform in a circular direction to "chase" a moving object.
The subject "chases" a moving point on the computer screen by tilting
the platform, attempting to keep the balance point near the moving
point on the computer screen. During the first three balance tests, the
computer screen was turned away from the subject so that visual feed-
back was less of a factor in enhancing position sense. During the dy-
namic test the subject must be able to see the screen to chase the ob-
ject. Order of the tests, positioning of the feet, and instructions were
the same for each subject. The balancing device was adjusted and cal-
ibrated for each subject depending on weight.

After the initial balance testing, the subjects were fatigued using an
isokinetic dynamometer (Cybex Kinetron II, Cybex, Ronkonkoma,
NY). This device imposes closed kinetic chain antagonistic exercise on
multiple joints, specifically the ankle, knee, and hip. The device, which
is similar to the well-known Stairmaster, forces eccentric and concent-
ric exercise on the hip, knee, and ankle flexor and extensor muscle
groups. Subjects were fatigued to less than 50% of their initial tested
strength, as determined by the force meter on the dynamometer. Fa-
tiguing exercise consisted of 1-min intervals at each of the following
 9/21

levels, with no rest between intervals, for a total of 10 min of exercise:

20 cm·s−1, 30 cm·s−1, 40 cm·s−1, 50 cm·s−1, 60 cm·s−1, 60 cm·s−1, 50
cm·s−1, 40 cm·s−1, 30 cm·s−1, and 20 cm·s−1. All subjects stated that
they felt significantly fatigued, but they were all able to complete the
protocol. The protocol consisted of balancing tests, which were done in
rapid sequence immediately following the fatiguing response. After
completing the exercise, each subject was then immediately retested
on the balance assessment system using the protocol as previously
described.

The data were analyzed statistically using repeated-measures ANOVA.

This test distinguishes variability between subjects from variability
within subjects, and it can be more powerful than an ordinary ANOVA
if pairing is effective. The post-hoc test was the Student-Newman-
Keuls multiple comparisons test to determine 95% confidence
intervals.

Back to Top

RESULTS

All 20 subjects completed the study. On completion of the fatigue por-

tion of the study, each subject stated that he or she was significantly
fatigued.

The unilateral, static, prefatigue right lower extremity balance test re-
vealed a mean score of 462.10 (range, 117-990). The postfatigue right
lower extremity mean score was 1014.55 (range, 286-2839). As stated
previously, the balance score is inversely proportional to balance skill,
with a higher score reflecting poorer balancing skills. The calculated P
value was <0.001 (Table 1).
 10/21

TABLE 1. Results of right unilateral static test on balancing device

pre- and postfatigue. Note: The lower the balancing score, the better
the balancing ability. Zero is a perfect score.

The unilateral, static, prefatigue left lower extremity balance test

demonstrated a mean score of 465.85 (range, 63-1206). The postfa-
tigue left lower extremity mean score was 1030.30 (range, 343-4322).
The P value was <0.001 (Table 2).

TABLE 2. Results of left unilateral static test on balancing device pre-

and postfatigue.

On the bilateral static test, the prefatigue mean balance score was
356.25 (range, 49-991). The bilateral postfatigue mean score was
869.30 (range, 348-1512). The P value was <0.001 (Table 3).
 11/21

TABLE 3. Results of bilateral static test on balancing device pre- and

postfatigue.

The prefatigue mean balance score for the dynamic study was 873.15
(range, 483-1708). Postfatigue, the mean balance score was 1105.85
(range, 552-1780). The P value was >0.05 (Table 4).

TABLE 4. Results of bilateral dynamic test on balancing device pre-

and postfatigue.

The repeated-measures ANOVA demonstrated significant differences

between pre- and postfatigue scores (P value < 0.0001) and confirmed
the effectiveness of the matching (P value < 0.0001). The Student-
Newman-Keuls multiple comparisons test was significant when pre-
and postfatigue scores were compared for the unilateral right (P value
< 0.001) and unilateral left (P value < 0.001) static tests and the bilat-
eral static test (P value < 0.001), but not significant when the pre- and
 12/21

postfatigue scores were compared for the dynamic test (P value >
0.05).

Back to Top

DISCUSSION

We measured the effects of lower extremity muscular fatigue on motor

control performance using a commercial balancing device. Fatigue sig-
nificantly decreased the ability of our subjects to balance on the balan-
cing device, especially in the first three balancing tests. The unilateral
and bilateral static tests demonstrated statistically significant worsen-
ing of balance skills.

The final balance test, the dynamic limb test, showed decreased motor
control performance after fatigue, but it was not significant. When re-
viewing the data from individual subjects, it is evident that in the dy-
namic portion of the test, some subjects were able to maintain their
balancing skills despite fatigue. There are several probable reasons for
this finding. During the dynamic testing, the subjects viewed the com-
puter screen to chase a moving object on the screen, thus providing
visual feedback to enhance lower limb position sense and motor con-
trol performance. When performing the first three balance tests, the
subjects were not allowed to see the computer screen, and hence there
was no visual feedback to augment proprioception. A second factor
that probably contributed to subjects not performing significantly
worse after fatigue as compared with the first three static tests is re-
covery. After the fatigue portion of the study, almost all subjects noted
that their lower extremities were very tired. However, some individu-
als stated that during the postfatigue portion of the balance testing,
their lower limbs felt as if they were recovering from the fatigue. This
 13/21

was noted especially during the last part of the balance testing, the dy-
namic test. Although subjective, it would appear that in our fatigue
model, some subjects were able to begin to recover from their fatigue
during the final parts of the balance testing.

The possibility that some subjects may recover from their fatigue
raises potential problems with this study's methodology. We put each
subject through the same rigorous 10-min workout and used a force
meter on the exercise machine to determine when individuals were us-
ing 50% or less force on the pedals. However, each individual's physic-
al ability and fitness level are different. Admittedly, our method of de-
termining fatigue was not quantitative, but for our purposes we be-
lieved it was adequate. The only factor that changed in our subjects
between the pre- and postfatigue portions of the balance tests was that
they were fatigued on the isokinetic dynamometer.

There are several possible reasons why muscular fatigue may affect
motor control ability. If the muscles were so fatigued that they were
unable to perform the physical task of balancing on the testing device,
then certainly balancing ability would be affected. However, all our
subjects were able to stand easily after the fatigue portion of the test,
and the act of balancing on the platform of the devices is, in and of it-
self, not physically demanding. Another explanation is that fatiguing
the muscles around a joint inhibits the joint's neuromuscular feedback
system. A synergism between joint proprioception and muscular func-
tion has been supported by several studies (4,5,13,18,20,21,25,32).
Our study does not specifically determine which aspect of the neur-
omuscular biofeedback loop is affected. Motor control of an extremity
is dependent upon afferent sensory and proprioceptive mechanore-
ceptors, such as Golgi tendon units, muscle spindles, and joint recept-
ors. It is also dependent upon efferent reflexive and voluntary muscu-
lar response. In our study we attempted to enhance proprioceptive de-
pendency to maintain balance by eliminating visual feedback, having
 14/21

the subject barefoot and not allowing arm movement to help with bal-
ancing. Visual feedback probably enhanced our subjects' performance
in the dynamic part of balance testing.

We cannot state definitively that fatigue affects proprioception.

However, it seems plausible that some form of muscle spindle desens-
itization or perhaps ligament relaxation and Golgi tendon desensitiza-
tion occurs with excessive fatigue. This may then lead to decreased ef-
ferent muscle response and poorer ability to maintain balance.

Our balance testing device, the unstable KAT platform, does not spe-
cifically measure proprioception as well as the device described by
Skinner et al (30). Perhaps future study to determine whether fatigue
specifically affects proprioception should be done using their apparat-
us. We do believe, however, that the KAT device does measure motor
control and balancing abilities and, by necessity, some element of
proprioceptive feedback because it is a part of the neuromuscular loop.
This is supported by the fact that ACL-deficient patients with known
proprioceptive deficits do poorly on their injured extremities when
tested on the unstable platform (24).

The data clearly support our hypothesis that fatigue can significantly
decrease balancing ability. This suggests that fatigued athletes may be
at increased risk of injury. Perhaps ligamentous laxity noted to occur
with fatigue also contributes to an increased incidence of injury (31).
Our findings corroborate the anecdotal evidence that ACL ruptures
and other knee injuries tend to occur near the end of a sporting event,
such as "the last run" when skiing (12). Certainly our data reinforce
what is already believed by many, that preconditioning and avoidance
of fatigue prevent injury.

These results also have important implications for rehabilitation in pa-

tients following cruciate ligament injury. Many authors believe that
 15/21

proprioceptive training plays a critical role in the rehabilitation of the

ACL-deficient or ACL-reconstructed knee (8,9,21,22,24,26,32,33). Sig-
nificant neurosensory deficit is known to accompany major joint in-
jury (7,14-16,19,26,29). It has been stated that the neuromuscular
feedback system plays an even greater role in the injured joint than in
the normal joint (16,18,32,33). Excessive fatiguing during rehabilita-
tion of an ACL-deficient or ACL-reconstructed knee may place the pa-
tient at greater risk of reinjury. We believe that in the early stages of
rehabilitation, specific neurosensory rehabilitation should be insti-
tuted aggressively. Proprioceptive training is necessary to overcome
the deficit associated with joint injury before progressing to high level
strengthening exercises. It is anticipated that such training will restore
normal kinematic and neuromuscular control patterns and reduce the
risk of reinjury.

In conclusion, we have demonstrated that fatigue significantly affects

the ability of an individual to maintain balance on an unstable plat-
form device. Fatigued individuals are probably at increased risk of
injury.

Back to Top

REFERENCES

1. Abramovici, A., I. Daizade, Z. Yosipovitch, et al. The distribution of

peptide containing nerves in the synovia of the cat knee joint. Histol.
Histopath. 6:469-476, 1991.
Cited Here...
2. Andrew, B. L. The sensory innervation of the medial ligament of the
knee joint. J. Physiol. 123:241-250, 1954.
Cited Here...
 16/21

3. Assimakopoulos, A. P., P. G. Katonis, M. V. Agapitos, and E. Ex-

archoul. The innervation of the human meniscus. Clin. Orthop.
275:232-236, 1992.
Cited Here...
4. Aune, A. K., L. Nordsletten, S. Skjeldal, J. E. Madsen, and A. Ede-
land. Hamstrings and gastrocnemius co-contraction protects the an-
terior cruciate ligament against failure: an in vivo study in the rat. J.
Orthop. Res. 13:147-150, 1995.
Cited Here...
5. Baratta, R., M. Solomonow, B. H. Zhou, D. Letson, R. Chuinard, and
R. D'Ambrosia. Muscular co-activation: the role of the antagonist
musculature in maintaining knee stability. Am. J. Sports Med.
16:113-122, 1988.
Cited Here...
6. Barrack, R. L., H. B. Skinner, and S. D. Cook. Proprioception of the
knee joint: paradoxical effect of training. Am. J. Phys. Med.
63:175-181, 1984.
Cited Here...
7. Barrack, R. L., H. B. Skinner, and S. L. Buckley. Proprioception in
the anterior cruciate deficient knee. Am. J. Sports Med. 17:1-6, 1989.
Cited Here...
8. Barrett, D. S., A. G. Cobb, and G. Bentley. Proprioception and func-
tion after anterior cruciate reconstruction. J. Bone Joint Surg.
73B:833-837, 1991.
Cited Here...
9. Day, R. W. and P. W. Byron. Proprioceptive training in the rehabilit-
ation of lower extremity injuries. Adv. Sports Med. Fitness 1:241-258,
1988.
Cited Here...
10. de Andrade, J. R., C. Grant, and A. S. J. Dixon. Joint distension
and reflex muscle inhibition in the knee. J. Bone Joint Surg.
47A:313-322, 1965.
Cited Here...
 17/21

11. Fahrer, H., H. U. Rentsch, N. J. Gerber, C. H. Beyler, C. H. W.

Hess, and B. Grüning. Knee effusion and reflex inhibition of the
quadriceps: a bar to effective retraining. J. Bone Joint Surg.
70B:635-638, 1988.
Cited Here...
12. Feagin, J. A., Jr., K. L. Lambert, R. R. Cunningham, et al. Consid-
eration of the anterior cruciate ligament injury in skiing. Clin. Orthop.
216:13-18, 1987.
Cited Here...
13. Ferrell, W. R., Jr., J. R. Rosenberg, R. H. Baxendale, D. Halliday,
and L. Wood. Fourier analysis of the relation between the discharge of
quadriceps motor units and periodic mechanical stimulation of cat
knee joint receptors. Exp. Physiol. 75:739-750, 1990.
Cited Here...
14. Fridën, T., R. Zätterström, A. Lindstrand, and U. Moritz. Disability
in anterior cruciate ligament insufficiency: an analysis of 19 untreated
patients. Acta Orthop. Scand. 61:131-135, 1990.
Cited Here...
15. Gauffin, H., G. Pettersson, Y. Tegner, and H. Tropp. Function test-
ing in patients with old rupture of the anterior cruciate ligament. Int.
J. Sports Med. 11:73-77, 1990.
Cited Here...
16. Gerber, C., H. Hoppeler, H. Claassen, G. Robotti, R. Zehnder, and
R. Jakob. The lower-extremity musculature in chronic symptomatic
instability of the anterior cruciate ligament. J. Bone Joint Surg.
67A:1034-1043, 1985.
Cited Here...
17. Grigg, P. Nervous system control of joint function. In: Biology and
Biomechanics of the Traumatized Synovial Joint: The Knee as a
Model. G. A. M. Finerman and F. R. Noyes (Eds.). American Academy
of Orthopaedic Surgeons: Rosemont, IL, 1992, pp. 275-287.
Cited Here...
 18/21

18. Johansson, H., P. Sjölander, and P. Sojka. A sensory role for the
cruciate ligaments. Clin. Orthop. 268:161-178, 1991.
Cited Here...
19. Johansson, H., P. Sjölander, and P. Sojka. Receptors in the knee
joint ligaments and their role in the biomechanics of the joint. Crit.
Rev. Biomed. Eng. 18:341-368, 1991.
Cited Here...
20. Kennedy, J. C., I. J. Alexander, and K. C. Hayes. Nerve supply of
the human knee and its functional importance. Am. J. Sports Med.
10:329-335, 1982.
Cited Here...
21. Lephart, S. M. and T. J. Henry. Functional rehabilitation for the
upper and lower extremity. Orthop. Clin. North Am. 26:579-592, 1995.
Cited Here...
22. Lephart, S. M., M. S. Kocher, F. H. Fu, et al. Proprioception follow-
ing anterior cruciate ligament reconstruction. J. Sports Rehab.
1:188-196, 1992.
Cited Here...
23. Losse, G. M., M. E. Howard, P. W. Cawley, et al. Correlation of
lower extremity injury to balance indices: an investigation utilizing an
instrumented unstable platform. Presented at the American Ortho-
paedic Society for Sports Medicine's Specialty Day, American
Academy of Orthopaedic Surgeons Annual Meeting, New Orleans, LA,
February 27, 1994.
Cited Here...
24. Losse, G. M., M. E. Howard, and P. W. Cawley. The effect of neuro-
sensory training following ACL reconstruction. Presented at the Amer-
ican Orthopaedic Society for Sports Medicine's Specialty Day, Americ-
an Academy of Orthopaedic Surgeons Annual Meeting, Atlanta, GA,
February 25, 1996.
Cited Here...
 19/21

25. Marshall, K. W. and W. G. Tatton. Joint receptors modulate short

and long latency muscle response in the awake cat. Exp. Brain Res.
83:137-150, 1990.
Cited Here...
26. Pitman, M. I., N. Nainzadeh, D. Menche, R. Gaselberti, and E. K.
Song. The intraoperative evaluation of the neurosensory function of
the anterior cruciate ligament in humans using somatosensory evoked
potentials. Arthroscopy 8:442-447, 1992.
Cited Here...
27. Ralphs, J. R. and M. Benjamin. The joint capsule: structure, com-
position, aging and disease. J. Anat. 184:503-509, 1994.
Cited Here...
28. Roland, P. E. and H. Ladegaard-Pedersen. A quantitative analysis
of sensations of tension and kinesthesia in man: evidence of a peri-
pherally originating muscular sense and for a sense effort. Brain
100:671-692, 1977.
Cited Here...
29. Schutte, M. J., E. J. Dabezies, M. L. Zimny, and L. T. Happel.
Neural anatomy of the human anterior cruciate ligament. J. Bone
Joint Surg. 69A:243-247, 1987.
Cited Here...
30. Skinner, H. B., R. L. Barrack, and S. D. Cook. Age-related decline
in proprioception. Clin. Orthop. 184:208-211, 1984.
Cited Here...
31. Skinner, H. B., M. P. Wyatt, M. L. Stone, J. A. Hodgdon, and R. L.
Barrack. Exercise-related knee joint laxity. Am. J. Sports Med.
14:30-34, 1986.
Cited Here...
32. Solomonow, M., R. Baratta, B. H. Zhou, et al. The synergistic ac-
tion of the anterior cruciate ligament and thigh muscles in maintain-
ing joint stability. Am. J. Sports Med. 15:207-213, 1987.
Cited Here...
 20/21

33. Zätterström, R., T. Fridén, A. Lindstrand, and U. Moritz. The effect

of physiotherapy on standing balance in chronic anterior cruciate liga-
ment insufficiency. Am. J. Sports Med. 22:531-536, 1994.
Cited Here...
Keywords:

FATIGUE; MOTOR CONTROL; INJURY

© Williams & Wilkins 1998. All Rights Reserved.

@Created by PDF to ePub