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Aftereffects of resisted muscle contractions on the accuracy of joint position sense in elite male athletes
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Aftereffects of Resisted Muscle Contractions on the Accuracy of Joint Position Sense in Elite Male Athletes Barry C. Stillman, FACP, MCSP, Joan M. McMeeken, MSc, Richard A.L. Macdonell, MD ABSTRACT. Stillman BC, McMeeken JM, Macdonell RAL. Aftereffects of resisted muscle contractions on the accuracy of joint position sense in elite male athletes. Arch Phys Med Rehabil 1998;79:1250-4.
Objective: To examine the effects of quadriceps and hamstring muscle strength testing on the results of subsequent knee joint position sense tests. Design: A case-control study of 40 elite male athletes divided equally into two groups, experimental and control. Methods: Both groups underwent position sense tests of both knees, with eyes closed, with isometric maintenance of the knee in each test position, return of the limb to the starting position, then active replication of the perceived test position using the same limb. In the experimental group, joint sense testing commenced 5 to 25min after strength testing of quadriceps and hamstring muscle strength in both legs using maximum isokinetic contractions at plateau speeds of 60°/sec and 120°/sec. The control group did not undergo pretest muscle strength testing. Results: The difference in the mean absolute (signless) and relative (signed) position sense errors between the experimental and control groups was 0.8 ° and 1.4 ° , respectively. The difference between the standard deviation of the relative errors was 1.2 °. These results were not statistically significant (analysis of variance p = .24,. 12, and. 13, respectively). Conclusion: In elite male athletes knee joint position sense is unaffected by nonfatiguing strength tests conducted 5 to 25rain before position sense testing. © 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation HE ACCURACY AND RELIABILITY of clinically asT sessed joint position sense may be influenced by a multitude of factors apart from the neuropathologic disorder under investigation. Among these factors is recent exercise of muscles crossing the joint to be examined. To date, three types of muscle contraction have been shown to influence the outcome of joint sense tests: (1) brief resisted isometric contractions, 1-4 (2) vibration induced muscle contractions (tonic vibration reflex), 1,2,5and (3) prolonged fatiguing contractions. 69 A brief resisted isometric contraction is followed by a sustained increase in the stretch reflex sensitivity of muscle spindles in the contracted m u s c l e . 1,3,1°-16 If, for example, the
From the School of Physiotherapy, The University of Melbourne (Mr. Stillman, Prof. McMeeken), and Department of Neurology, Austin and Repatriation Medical Centre (Dr. Macdonell), Victoria, Australia. Submitted for publication November 13, 1997. Accepted in revised form April 10, 1998. No commercial patty having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Barry Stillman, School of Physiotherapy, The University of Melbourne, 200 Berkeley Street, Carlton, Victoria, Australia 3052. © 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation 0003-9993/98/7910-471953.00/0
Arch Phys Med Rehabil Vol 79, October 1998
elbow is slowly and passively moved to an extended position following an isometric contraction of the biceps brachii muscle, the subject is left with a perception of the elbow being more extended than its actual final position. This sensory illusion has been widely attributed to a persisting contraction of intrafusal fibers of the muscle spindles within the previously contracted muscle with a consequent enhanced sensitivity of the spindle primary endings. 17 Subsequent repositioning of the joint to place the muscle in a lengthened position, as in the above example, is then interpreted as a greater-than-actual stretch of the muscle, and the subject consequently perceives the underlying joint to be more extended than it actually is. Other, possibly coexisting effects include persistent postcontractional "changes in the central mechanisms which process proprioceptive inputs. ''2 A similar disturbance of joint sense, probably with a similar mechanism, has been observed when the tonic vibration reflex is substituted for a resisted isometric contraction. 1,2 Both the postcontractional and postvibratory illusory effects may persist for several minutes. 1,18,19 With one exception, where the findings were inconsistent, 2° other studies have demonstrated reduced joint sense after prolonged, fatiguing muscle exercise. 69 At present the possible mechanisms for this effect are somewhat speculative. It has been postulated that there are three broad categories of neural effects: (1) altered sensory feedback from the fatigued muscles, (2) altered neuronal excitability in the spinal cord, and (3) altered supraspinal excitation of spinal neurons.21,22 Increased Ia afferent discharge from muscle spindles in the fatigued muscles occurring shortly after fatigue, 22,23 and later increases in group III and IV afferent activity secondary to the metabolic effects of the exercise, 2z24,25 may influence joint sense in the fatigued muscles by acting on spinal interneurons that form part of the ascending proprioceptive afferent fiber system, or by changing the kinesthetic acuity of overlying muscles by acting on their fusirnotor neurons and thus muscle spindle afferent discharge56 In the study by Brockett and associates, 9 disturbed knee joint sense was demonstrated for up to four days after fatiguing eccentric quadriceps muscle exercise. During rehabilitation a clinician might test joint sense shortly after a period of intense exercise, or after a session of strength or endurance testing. The above studies suggest that such joint position sense tests could produce abnormal or atypical test results. It remains unclear, however, whether nonfatiguing exercise might also affect joint sense test results. Although nonfatiguing exercise or strength testing would not be expected to evoke the abovementioned intramuscular metabolic effects, there could be enduring spinal or supraspinal neuronal adaptations. The present study set out to investigate this possibility in a group of elite athletes. The subjects, all participants in Australian Rules football at the national level, were chosen because they were a homogeneous group familiar with and highly motivated to undertake exercise and testing procedures, with a similar high level of physical fitness that would make it unlikely for them to be fatigued by the proposed strength testing protocol.
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METHODS Subjects Forty healthy male subjects provided informed written consent in accordance with the requirements of the Ethics Committee of The University of Melbourne. All subjects participated in Australian Rules Football at the national level and thus may be classed as elite athletes. By questionnaire, interview, and clinical examination when appropriate, it was established that no subject had current evidence of injury or other abnormality affecting the knee joints or surrounding muscles. The experimental group (n = 20), had position sense tested in both knees shortly after a strength testing program. These subjects' mean age was 24.1yrs _ 3.7yrs (SD). A second (control) group of 20 subjects, who had no strength testing, had a mean age of 21.4yrs -+ 2.9yrs (SD).
Procedure The maximum concentric and eccentric strengths of the quadriceps and hamstring muscles were determined in both legs of subjects in the experimental group using a Kin-Corn electromechanical isokinetic dynamometer? The subjects were seated, and all tests were conducted over the arc between approximately 5 ° and 95 ° flexion with 0 ° representing the straight knee position. The quadriceps and hamstring muscle groups were each tested by concentric and eccentric isokinetic contractions at plateau speeds of 60°/sec and 120°/sec. The order of testing the lower limbs was alternated between subjects. The test of concentric quadriceps contractions at 60°/sec was preceded by a familiarization and warmup of 10 concentric quadriceps contractions at 60°/sec and 25% of maximum voluntary effort. The warmup was followed by one concentric quadriceps contraction at 60°/sec and 75% of maximum voluntary effort. This was followed by at least three maximumeffort repetitions. The object was to determine the maximum voluntary torque during three consecutive maximum-effort repetitions that showed minimal differences between the muscle outputs. Accordingly each subject produced at least three, and often four or five, maximum-effort repetitions of the quadriceps concentric exercise at 60°/sec. The above procedure, including warmup was repeated for the quadriceps and hamstring muscle groups on both limbs, contracting concentrically and eccentrically, and at the two chosen plateau speeds. In the experimental group a period not exceeding 5min elapsed between the end of the final strength test and the start of the first position sense test. For the joint sense tests, right and left knee position sense was tested actively, after which the limb was returned to the starting position before the subjects attempted to replicate the test position using the same limb. The order of testing the two knees was alternated between subjects. All subjects were seated on the side of a couch with the trunk inclined approximately 70 ° to the horizontal, and with folded towels behind the knees so that the thighs were horizontal. The knees were flexed over the couch edge at a starting position of about 80 ° flexion. Two reflective markers were positioned on the thigh, one over the greater trochanter and one over the lower end of the iliotibial tract; and two on the leg, one over the anterior border of the neck of fibula and one over the lateral malleolus (fig 1). These markers were used to facilitate subsequent computer digitization of the various sagittal knee positions recorded on videotape throughout the procedure. Each test or response position was determined as the average of 16 consecutive knee angles digitized at 50Hz from the videotape view of each position.
Fig 1. Sagittal placement of reflective markers and video camera field of view for computer-determined knee joint test and response positions.
The choice of marker positions was based on studies by Lafortune and colleagues 27 and others who have shown that the skin marker movement over the lateral condylar region of the knee increases as the lower thigh marker is placed closer to the line of the knee joint, and by Tully and Stillman28 who also clarified optimum placement for the other three markers. The so-called iliotibial tract marker is sufficiently proximal to minimize underlying skin movement, and the neck of fibular marker, when combined with the lateral malleolus, represents the axis of the leg more validly than does the more traditional head-of-fibula marker. This form of video image goniometry of knee flexion-extension has proved to be reliable and accurate to about 1.4 °. Three test positions were investigated at each knee. With the subject's eyes closed and the lower limb relaxed the examiner passively extended the knee to the chosen test position, about 20 ° , 40 ° and 60 ° flexion, as judged subjectively by the examiner, then instructed the subject to hold the knee (isometrically) in that position. The examiner's hand support was discontinued and each subject held the knee for about 5sec. After the limb was returned to the starting position the subject was instructed to attempt to actively return the limb to the perceived test position.
Statistical Analysis For each position sense test the relative error was determined as the arithmetic difference between the computed test position and the response position, with positive errors representing overestimation (ie, a response position with the knee more extended than the test position). The absolute error (ie, the signless difference between test and response positions) was also calculated; before statistical analysis researchers determined the mean of the six relative errors obtained on the three tests of the left knee and three of the right knee, the mean of the six absolute errors, and the standard deviation of the six relative errors. These subject-averaged results were then used in comparisons of the joint sense errors in the experimental and control groups. Comparisons were by factorial analysis of variance with the probability level set at .05.
RESULTS Results from the three position sense measures are summarized by group in table 1. Although errors in the experimental group were smaller, the difference compared to the control group was not statistically significant (table 2). Arch Phys Med Rehabil Vol 79, October 1998
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Table 1: Errors in Perceived Knee Position Following Active Knee Joint Position Sense Tests With Ipsilateral Matching Responses Group
Relative Error (°)
Absolute Error (°)
Variable Error (°)
Control* (n = 20) Experimental* (n = 20)
3.9 -+ 3.1 2.5 _+ 2.9
4.9 + 2.7 4.1 +- 1.4
4.5 3.3
Values for relative error and absolute error are presented as means -+ standard deviation (SD). Values for variable error are presented as means of SDs of relative errors. * Did not undergo muscle strength testing before the position sense tests. * Underwent quadriceps and hamstring muscle strength tests before the position sense tests.
DISCUSSION Relatively few studies have related joint sense test results to various types of preceding exercise. All types of exercise have not been evaluated, and those that have, have not revealed the answers to several important questions. Regarding the acute aftereffects of isometric contraction, increased muscle spindle excitability may be avoided by moving the previously contracted muscle to a shortened length, 1 or by stretching the previously contracted muscle. 15,29-31Before joint sense testing, a clinician might easily ensure that no residual post-isometric contraction effects occur by producing, for example, several alternating active flexion-extension movements at the joint, or by alternating passive joint movements. If, however, the illusory aftereffects of muscle contraction involve spinal neuronal pool changes, such centrally mediated aftereffects might not be so easily extinguished. Perhaps they may only be avoided by allowing sufficient time for the effects to decay to zero. The details of the temporal decay of the postcontractional illusory effects remain to be clarified. The purpose of the present study was twofold. The first aim was to investigate possible central spinal neuronal aftereffects following nonisometric and nonfatiguing strength testing which nevertheless incorporated maximally resisted dynamic (isokinetic) muscle contractions. A second aim was to gain further insight into the period of elapsed time before joint sense can be tested without fear of the results being contaminated by the preceding muscle contractions. Although fatigue was not quantitatively evaluated after the strength testing program, this program contained no prolonged contractions of the endurance type, and the subjective impression of lack of discomfort voiced by each volunteer immediately prior to position sense testing suggested that the thigh muscles were not fatigued at the time of the joint position sense tests. Recall that all of these subjects were elite athletes accustomed to regular and intense exercise. Consequently it was assumed that there was little likelihood of the intramuscular chemical changes of the type that might follow fatiguing exercise. Moreover, because the muscles were contracted concentrically and eccentrically during the strength testing protocol, muscle spindle sensitivity changes of the type that follow isometric contractions were not likely. However spinal interneuronal and fusimotoneuronal pool sensitivity changes during and following the strength testing protocol was considTable 2: Analysis of Variance Between Position Sense Errors Produced by Experimental and Control Groups Factor
FStatistic
p
Significance
Relative error Absolute error Variable error
2.49 1.44 2.43
.12 .24 .13
None None None
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ered a possibility, particularly since Hutton's group 29 showed that stretch following brief isometric exercise fails to completely restore normal proprioceptive sensibility. The negative results from the present study suggest that there were no persisting effects from the strength testing program of sufficient magnitude to enhance or suppress joint position sense. If there was to be an effect, based on the abovementioned studies, the expectation would be of a reduced joint sense, whereas the present study revealed a statistically insignificant enhanced joint sense. Perhaps a larger series of subjects will reveal that the nonspecific warmup or arousal effects of nonfatiguing exercise favour enhanced joint sense. It may also be asked to what extent these results derived from elite male athletes translate to healthy nonathletes, or rehabilitation patients with various neuromuscular disorders. Evidence supporting the proposition that elite athletes might have superior levels of joint sense compared to all others, either through genetic good fortune or as an acquired capability following years of sporting participation, is minimal and equivocal. While two studies of position sense tests have suggested that various categories of sportspersons have superior joint sense, 31,32 an unpublished study by the present authors found no significant difference in position sense accuracy or variability when active position sense tests results from 43 elite Australian Rules footballers were compared to the results from 16 age-matched control subjects (including 14 women). While a few studies have provided evidence of spinal proprioceptive adaptations to chronic exercise in experimental animals and sportspersons, 33 these adaptations are modest and involve an enhancement rather than a fundamental change in the pertinent peripheral and central neurobiology; therefore, it is likely that the neural mechanisms underpinning the present study are also present in the general population, but patients with various types of motor disorder from neurological dysfunction might not manifest the same kinesthetic response following strength testing or exercise. This difference, if there is one, is more likely to be related to a greater propensity to fatigue. It is postulated that patients with an intact nervous system are unlikely to manifest a fundamentally different kinesthetic response to nonfatiguing exercise. Until this matter is further clarified, it can only be recommended that clinicians be cautious about kinesthetic assessment shortly after a period of presumed nonfatiguing strength testing or exercise, and postpone kinesthetic tests following fatiguing contractions. In the present study both lower limbs were strength tested, and the order of limb testing was alternated during both the strength and joint sense tests; consequently, different periods of time elapsed between the offset of strength testing one limb, and the onset of position sense testing the same limb. Based on the average duration of the strength tests and position sense tests, the longest interval between strength test and position sense test of the same limb could have been 25min (eg, when the right (left) knee was strength tested first and position sense tested last). The shortest interval was less than 5min, therefore, it may be argued that in some limbs an acute potcontractional sensory effect may have been extinguished with time before the onset of position sense testing. Based on the present study one may argue 25min is the minimum time that may elapse between the offset strength testing and the onset of position sense tests without concern for contaminating postexercise effects. The subjects in this study all participated in a near-identical long-term fitness and skill training program, which caused the authors to conclude that their level of thigh muscle strength was both relatively similar and abnormally high. The strength testing program required each subject to perform maximum
AFTEREFFECTS OF EXERCISE ON JOINT SENSE, Stillman
voluntary contractions. This ensured that the difficulty level of the strength testing program was similar for all subjects. Moreover, as previously noted, the regime was not evidently taxing for any of the subjects. The general applicability of the experimental findings might conceivably be expanded by investigating the proprioceptive effects from different submaxireal levels of thigh muscle contractions; however the likelihood that nonfatiguing submaximal exercise regimes will interfere with subsequently tested joint position sense, when a maximum strength testing regime did not, seems remote. CONCLUSION The present study has shown that a regime of nonfatiguing nontraumatic maximally-resisted concentric and eccentric isokinetic quadriceps and hamstring contractions, occupying about 15rain per limb, had no statistically significant effect on either the accuracy (as evidenced by the relative and absolute errors) or precision (as evidenced by the variable errors) of knee joint position sense tested within 5 to 25rain of the offset of the strength tests. Since the presence and time course of postcontractional illusory effects remains to be fully elucidated, and in the present experiment there may have been hidden acute effects, it would be of value to extend the present study using only one lower limb so that the elapsed period before position sense testing could be systematically varied; for example, between 0 and 20rain. The findings from such a study might be enhanced by varying the number of repetitions in the exercise program to have nonfatigued, mildly fatigued, and markedly fatigued subgroups. Also, examination of different subject groups, including patients with broad-ranging disturbances of motor function, will be necessary to broaden the context of this area of investigation. It would also be of value both in sport and in rehabilitation medicine to clarify what forms of intervention can be used to extinguish the aftereffects of fatiguing exercise on joint sense. For example, joint sense disturbances following fatigue in sport might be a factor in precipitating sporting injuries. Are there simple strategies such as a period of unresisted reciprocal exercise--peddling a stationary bicycle, for example--that might be used to maintain or restore high levels of joint sense acuity following fatiguing exercise? The present study has added one additional piece of information to this emerging story of the relationship between exercise and kinesthetic acuity.
Acknowledgment: The authors thank Dr Kim Bennell for her assistance in recruiting subjects. References 1. Gregory JE, Morgan DL, Proske U. Aftereffects in the responses of cat muscle spindles and errors of limb position sense in man. J Neurophysiol 1988;59:1220-30. 2, Gilhodes JC, Gurfinkel VS, Roll JP. Role of Ia muscle spindle afferents in post-contraction and post-vibration motor effect genesis. Neurosci Lett 1992;135:247-51. 3. Proske U, Morgan DL, Gregory JE. Muscle history dependence of responses to stretch of primary and secondary endings of cat soleus muscle spindles. J Physiol 1992;445:81-95. 4. Wise AK, Gregory JE, Proske U. The effects of muscle conditioning on movement detection thresholds at the human forearm. Brain Res 1996;735:125-30. 5. Rogers DK, Bendrups AP, Lewis MM. Disturbed proprioception following a period of muscle vibration in humans. Neurosci Lett 1985;57:147-52.
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6. Skinner HB, Wyatt MR Hodgdon JA, Conard DW, Barrack RL. Effect of fatigue on joint position sense of the knee. J Orthop Res 1986;4:l 12-8. 7. Marks R, Quinney HA. Effect of fatiguing maximal isokinetic quadriceps contractions on ability to estimate knee position. Percept Mot Skills 1993;77:1195-1202. 8. Marks R. Effect of exercise-induced fatigue on position sense of the knee. Aust J Physiother 1994;40:175-81. 9. Brockett C, Warren N, Gregory JE, Morgan DL, Proske U. A comparison of the effects of concentric versus eccentric exercise on force and position sense at the human elbow joint. Brain Res 1997;771:251-8. 10. Enoka RM, Hutton RS, Eldred E. Changes in excitability of tendon tap and Hoffman reflexes following voluntary contractions. Electroencephalog Clin Neurophysiol 1980;48:664-72. 11. Hagbarth K-E, H~igglundJV, Nordin M, Wallin EU. Thixotropic behavior of human finger flexor muscles with accompanying changes in spindle and reflex responses to stretch. J Physiol 1985;368:323-42. 12. Hagbarth K-E, Nordin M, Bongiovanni LG. After-effects on stiffness and stretch reflexes of human finger flexor muscles attributed to muscle thixotropy. J Physiol 1995;482:215-23. 13. Gregory JE, Morgan DL, Proske U. Changes in size of the stretch reflex of cat and man attributed to aftereffects in muscle spindles. J Neurophysiol 1987;58:628-39. 14. Gregory JE, Mark RF, Morgan DL, Patac A, Polus B, Proske U. Effects of movement history on the stretch reflex in cat and man. J Physiol 1990;424:93-107. 15. Jahnke MT, Proske U, S~uppler A. Measurements of muscle stiffness, the electromyogram and activity in single muscle spindles of human flexor muscles following conditioning by passive stretch or contraction. Brain Res 1989;493:103-12. 16. Ribot-Ciscar E, Tardy-Gervet MF, Vedel JR Roll JR Postcontraction changes in human muscle spindle resting discharge and stretch sensitivity. Exp Brain Res 1991;86:673-8. 17. ProskeU, Morgan DL, Gregory JE. Thixotrophy in skeletal muscle and in muscle spindles: A review. Progr Neurobiol 1993;41:70521. 18. Marsden CD, Meadows JC, Hodgson HJF. Observations on the reflex response to muscle vibration in man and its voluntary control. Brain 1969;92:829-46. 19. Rogers DK, Bendrups AR Lewis MM. Disturbed proprioception following a period of muscle vibration in humans. Neurosci Lett 1985;57:147-52. 20. Sharpe MH, Miles TS. Position sense at the elbow after fatiguing contractions. Exp Brain Res 1993;94:179-82. 21. Enoka RM, Stuart DG. Neurobiology of muscle fatigue. J Appl Physiol 1992;72:1631-48. 22. Gandevia SC. Neuromuscular fatigue mechanisms: Central and peripheral factors affecting motoneuronal output in fatigue. In: Victoria University of Technology, editor. Fatigue in sports and exercise. Footscray: Victoria University of Technology; 1990. p. 9-15. 23. Kirsch RF, Rymer WZ. Neural compensation of muscular fatigue: Evidence for significant force regulation in man. J Neurophysiol 1987;57:1893-910. 24. Bigland-Ritchie B, Dawson NJ, Johansson RS, Lippold OCJ. Origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. J Physiol 1986;379:451-9. 25. Darques JL, Jammes Y. Fatigue-induced changes in group IV muscle afferent activity: Differences between high- and lowfrequency electrically induced fatigues. Brain Res 1996;750:14754. 26. Johansson H, Sj61anderE Neurophysiology of joints. In: Wright V, Radin E, editors. The mechanics of human joints: Physiology, pathophysiology and treatment. New York: Dekker; 1993. p. 243-90. 27. Lafortune MA, Lambert C, Lake M. Skin marker displacement at the knee joint. Proceedings of NACOB II. The Second North Arch Phys Med Rehabil Vol 79, October 1998
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American Congress on Biomechanics; 1992 Aug 24-28; Chicago. Chicago: NACOB; 1992. p. 101-2. 28. Tully E, Stillman B. A revised model for 2D kinematic analysis of spine, hip and knee motion in the sagittal plane. In: Proceedings of the Twelth World Congress of Physical Therapy. Washington (DC): World Congress of Physical Therapy. 1995. p. 732. 29. Hutton RS, Kaiya K, Suzuki S, Watanabe S. Post-contraction errors in human force production are reduced by muscle stretch. J Physiol 1987;393:247-59. 30. Baumann TK, Emonet-D6nand E Hulliger M. After-effects of fusimotor stimulation on spindle Ia afferents' dynamic sensitivity, revealed during slow movements. Brain Res 1982;232:460-5.
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31. Euzet J-P, Gah6ry Y. Relationships between position sense and physical practice. J Hum Move Studies 1995;28:149-73. 32. Jerosch J, Prymka M. Proprioception and joint stability, Knee surgery, Sports Traumatol Arthrosc 1996;4:171-9. 33. Hutton RS, Atwater SW. Acute and chronic adaptations of muscle proprioceptors in response to increased use. Sports Med 1992;14: 406-21.
Supplier a. Kinetic communicator (KIN-COM); Chattanooga Instruments, Inc., 101 Memorial Drive, Chattanooga, TN 37405.
Aftereffects of Resisted Muscle Contractions on the Accuracy of Joint Position Sense in Elite Male Athletes Barry C. Stillman, FACP, MCSP, Joan M. McMeeken, MSc, Richard A.L. Macdonell, MD ABSTRACT. Stillman BC, McMeeken JM, Macdonell RAL. Aftereffects of resisted muscle contractions on the accuracy of joint position sense in elite male athletes. Arch Phys Med Rehabil 1998;79:1250-4.
Objective: To examine the effects of quadriceps and hamstring muscle strength testing on the results of subsequent knee joint position sense tests. Design: A case-control study of 40 elite male athletes divided equally into two groups, experimental and control. Methods: Both groups underwent position sense tests of both knees, with eyes closed, with isometric maintenance of the knee in each test position, return of the limb to the starting position, then active replication of the perceived test position using the same limb. In the experimental group, joint sense testing commenced 5 to 25min after strength testing of quadriceps and hamstring muscle strength in both legs using maximum isokinetic contractions at plateau speeds of 60°/sec and 120°/sec. The control group did not undergo pretest muscle strength testing. Results: The difference in the mean absolute (signless) and relative (signed) position sense errors between the experimental and control groups was 0.8 ° and 1.4 ° , respectively. The difference between the standard deviation of the relative errors was 1.2 °. These results were not statistically significant (analysis of variance p = .24,. 12, and. 13, respectively). Conclusion: In elite male athletes knee joint position sense is unaffected by nonfatiguing strength tests conducted 5 to 25rain before position sense testing. © 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation HE ACCURACY AND RELIABILITY of clinically asT sessed joint position sense may be influenced by a multitude of factors apart from the neuropathologic disorder under investigation. Among these factors is recent exercise of muscles crossing the joint to be examined. To date, three types of muscle contraction have been shown to influence the outcome of joint sense tests: (1) brief resisted isometric contractions, 1-4 (2) vibration induced muscle contractions (tonic vibration reflex), 1,2,5and (3) prolonged fatiguing contractions. 69 A brief resisted isometric contraction is followed by a sustained increase in the stretch reflex sensitivity of muscle spindles in the contracted m u s c l e . 1,3,1°-16 If, for example, the
From the School of Physiotherapy, The University of Melbourne (Mr. Stillman, Prof. McMeeken), and Department of Neurology, Austin and Repatriation Medical Centre (Dr. Macdonell), Victoria, Australia. Submitted for publication November 13, 1997. Accepted in revised form April 10, 1998. No commercial patty having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Barry Stillman, School of Physiotherapy, The University of Melbourne, 200 Berkeley Street, Carlton, Victoria, Australia 3052. © 1998 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation 0003-9993/98/7910-471953.00/0
Arch Phys Med Rehabil Vol 79, October 1998
elbow is slowly and passively moved to an extended position following an isometric contraction of the biceps brachii muscle, the subject is left with a perception of the elbow being more extended than its actual final position. This sensory illusion has been widely attributed to a persisting contraction of intrafusal fibers of the muscle spindles within the previously contracted muscle with a consequent enhanced sensitivity of the spindle primary endings. 17 Subsequent repositioning of the joint to place the muscle in a lengthened position, as in the above example, is then interpreted as a greater-than-actual stretch of the muscle, and the subject consequently perceives the underlying joint to be more extended than it actually is. Other, possibly coexisting effects include persistent postcontractional "changes in the central mechanisms which process proprioceptive inputs. ''2 A similar disturbance of joint sense, probably with a similar mechanism, has been observed when the tonic vibration reflex is substituted for a resisted isometric contraction. 1,2 Both the postcontractional and postvibratory illusory effects may persist for several minutes. 1,18,19 With one exception, where the findings were inconsistent, 2° other studies have demonstrated reduced joint sense after prolonged, fatiguing muscle exercise. 69 At present the possible mechanisms for this effect are somewhat speculative. It has been postulated that there are three broad categories of neural effects: (1) altered sensory feedback from the fatigued muscles, (2) altered neuronal excitability in the spinal cord, and (3) altered supraspinal excitation of spinal neurons.21,22 Increased Ia afferent discharge from muscle spindles in the fatigued muscles occurring shortly after fatigue, 22,23 and later increases in group III and IV afferent activity secondary to the metabolic effects of the exercise, 2z24,25 may influence joint sense in the fatigued muscles by acting on spinal interneurons that form part of the ascending proprioceptive afferent fiber system, or by changing the kinesthetic acuity of overlying muscles by acting on their fusirnotor neurons and thus muscle spindle afferent discharge56 In the study by Brockett and associates, 9 disturbed knee joint sense was demonstrated for up to four days after fatiguing eccentric quadriceps muscle exercise. During rehabilitation a clinician might test joint sense shortly after a period of intense exercise, or after a session of strength or endurance testing. The above studies suggest that such joint position sense tests could produce abnormal or atypical test results. It remains unclear, however, whether nonfatiguing exercise might also affect joint sense test results. Although nonfatiguing exercise or strength testing would not be expected to evoke the abovementioned intramuscular metabolic effects, there could be enduring spinal or supraspinal neuronal adaptations. The present study set out to investigate this possibility in a group of elite athletes. The subjects, all participants in Australian Rules football at the national level, were chosen because they were a homogeneous group familiar with and highly motivated to undertake exercise and testing procedures, with a similar high level of physical fitness that would make it unlikely for them to be fatigued by the proposed strength testing protocol.
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METHODS Subjects Forty healthy male subjects provided informed written consent in accordance with the requirements of the Ethics Committee of The University of Melbourne. All subjects participated in Australian Rules Football at the national level and thus may be classed as elite athletes. By questionnaire, interview, and clinical examination when appropriate, it was established that no subject had current evidence of injury or other abnormality affecting the knee joints or surrounding muscles. The experimental group (n = 20), had position sense tested in both knees shortly after a strength testing program. These subjects' mean age was 24.1yrs _ 3.7yrs (SD). A second (control) group of 20 subjects, who had no strength testing, had a mean age of 21.4yrs -+ 2.9yrs (SD).
Procedure The maximum concentric and eccentric strengths of the quadriceps and hamstring muscles were determined in both legs of subjects in the experimental group using a Kin-Corn electromechanical isokinetic dynamometer? The subjects were seated, and all tests were conducted over the arc between approximately 5 ° and 95 ° flexion with 0 ° representing the straight knee position. The quadriceps and hamstring muscle groups were each tested by concentric and eccentric isokinetic contractions at plateau speeds of 60°/sec and 120°/sec. The order of testing the lower limbs was alternated between subjects. The test of concentric quadriceps contractions at 60°/sec was preceded by a familiarization and warmup of 10 concentric quadriceps contractions at 60°/sec and 25% of maximum voluntary effort. The warmup was followed by one concentric quadriceps contraction at 60°/sec and 75% of maximum voluntary effort. This was followed by at least three maximumeffort repetitions. The object was to determine the maximum voluntary torque during three consecutive maximum-effort repetitions that showed minimal differences between the muscle outputs. Accordingly each subject produced at least three, and often four or five, maximum-effort repetitions of the quadriceps concentric exercise at 60°/sec. The above procedure, including warmup was repeated for the quadriceps and hamstring muscle groups on both limbs, contracting concentrically and eccentrically, and at the two chosen plateau speeds. In the experimental group a period not exceeding 5min elapsed between the end of the final strength test and the start of the first position sense test. For the joint sense tests, right and left knee position sense was tested actively, after which the limb was returned to the starting position before the subjects attempted to replicate the test position using the same limb. The order of testing the two knees was alternated between subjects. All subjects were seated on the side of a couch with the trunk inclined approximately 70 ° to the horizontal, and with folded towels behind the knees so that the thighs were horizontal. The knees were flexed over the couch edge at a starting position of about 80 ° flexion. Two reflective markers were positioned on the thigh, one over the greater trochanter and one over the lower end of the iliotibial tract; and two on the leg, one over the anterior border of the neck of fibula and one over the lateral malleolus (fig 1). These markers were used to facilitate subsequent computer digitization of the various sagittal knee positions recorded on videotape throughout the procedure. Each test or response position was determined as the average of 16 consecutive knee angles digitized at 50Hz from the videotape view of each position.
Fig 1. Sagittal placement of reflective markers and video camera field of view for computer-determined knee joint test and response positions.
The choice of marker positions was based on studies by Lafortune and colleagues 27 and others who have shown that the skin marker movement over the lateral condylar region of the knee increases as the lower thigh marker is placed closer to the line of the knee joint, and by Tully and Stillman28 who also clarified optimum placement for the other three markers. The so-called iliotibial tract marker is sufficiently proximal to minimize underlying skin movement, and the neck of fibular marker, when combined with the lateral malleolus, represents the axis of the leg more validly than does the more traditional head-of-fibula marker. This form of video image goniometry of knee flexion-extension has proved to be reliable and accurate to about 1.4 °. Three test positions were investigated at each knee. With the subject's eyes closed and the lower limb relaxed the examiner passively extended the knee to the chosen test position, about 20 ° , 40 ° and 60 ° flexion, as judged subjectively by the examiner, then instructed the subject to hold the knee (isometrically) in that position. The examiner's hand support was discontinued and each subject held the knee for about 5sec. After the limb was returned to the starting position the subject was instructed to attempt to actively return the limb to the perceived test position.
Statistical Analysis For each position sense test the relative error was determined as the arithmetic difference between the computed test position and the response position, with positive errors representing overestimation (ie, a response position with the knee more extended than the test position). The absolute error (ie, the signless difference between test and response positions) was also calculated; before statistical analysis researchers determined the mean of the six relative errors obtained on the three tests of the left knee and three of the right knee, the mean of the six absolute errors, and the standard deviation of the six relative errors. These subject-averaged results were then used in comparisons of the joint sense errors in the experimental and control groups. Comparisons were by factorial analysis of variance with the probability level set at .05.
RESULTS Results from the three position sense measures are summarized by group in table 1. Although errors in the experimental group were smaller, the difference compared to the control group was not statistically significant (table 2). Arch Phys Med Rehabil Vol 79, October 1998
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Table 1: Errors in Perceived Knee Position Following Active Knee Joint Position Sense Tests With Ipsilateral Matching Responses Group
Relative Error (°)
Absolute Error (°)
Variable Error (°)
Control* (n = 20) Experimental* (n = 20)
3.9 -+ 3.1 2.5 _+ 2.9
4.9 + 2.7 4.1 +- 1.4
4.5 3.3
Values for relative error and absolute error are presented as means -+ standard deviation (SD). Values for variable error are presented as means of SDs of relative errors. * Did not undergo muscle strength testing before the position sense tests. * Underwent quadriceps and hamstring muscle strength tests before the position sense tests.
DISCUSSION Relatively few studies have related joint sense test results to various types of preceding exercise. All types of exercise have not been evaluated, and those that have, have not revealed the answers to several important questions. Regarding the acute aftereffects of isometric contraction, increased muscle spindle excitability may be avoided by moving the previously contracted muscle to a shortened length, 1 or by stretching the previously contracted muscle. 15,29-31Before joint sense testing, a clinician might easily ensure that no residual post-isometric contraction effects occur by producing, for example, several alternating active flexion-extension movements at the joint, or by alternating passive joint movements. If, however, the illusory aftereffects of muscle contraction involve spinal neuronal pool changes, such centrally mediated aftereffects might not be so easily extinguished. Perhaps they may only be avoided by allowing sufficient time for the effects to decay to zero. The details of the temporal decay of the postcontractional illusory effects remain to be clarified. The purpose of the present study was twofold. The first aim was to investigate possible central spinal neuronal aftereffects following nonisometric and nonfatiguing strength testing which nevertheless incorporated maximally resisted dynamic (isokinetic) muscle contractions. A second aim was to gain further insight into the period of elapsed time before joint sense can be tested without fear of the results being contaminated by the preceding muscle contractions. Although fatigue was not quantitatively evaluated after the strength testing program, this program contained no prolonged contractions of the endurance type, and the subjective impression of lack of discomfort voiced by each volunteer immediately prior to position sense testing suggested that the thigh muscles were not fatigued at the time of the joint position sense tests. Recall that all of these subjects were elite athletes accustomed to regular and intense exercise. Consequently it was assumed that there was little likelihood of the intramuscular chemical changes of the type that might follow fatiguing exercise. Moreover, because the muscles were contracted concentrically and eccentrically during the strength testing protocol, muscle spindle sensitivity changes of the type that follow isometric contractions were not likely. However spinal interneuronal and fusimotoneuronal pool sensitivity changes during and following the strength testing protocol was considTable 2: Analysis of Variance Between Position Sense Errors Produced by Experimental and Control Groups Factor
FStatistic
p
Significance
Relative error Absolute error Variable error
2.49 1.44 2.43
.12 .24 .13
None None None
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ered a possibility, particularly since Hutton's group 29 showed that stretch following brief isometric exercise fails to completely restore normal proprioceptive sensibility. The negative results from the present study suggest that there were no persisting effects from the strength testing program of sufficient magnitude to enhance or suppress joint position sense. If there was to be an effect, based on the abovementioned studies, the expectation would be of a reduced joint sense, whereas the present study revealed a statistically insignificant enhanced joint sense. Perhaps a larger series of subjects will reveal that the nonspecific warmup or arousal effects of nonfatiguing exercise favour enhanced joint sense. It may also be asked to what extent these results derived from elite male athletes translate to healthy nonathletes, or rehabilitation patients with various neuromuscular disorders. Evidence supporting the proposition that elite athletes might have superior levels of joint sense compared to all others, either through genetic good fortune or as an acquired capability following years of sporting participation, is minimal and equivocal. While two studies of position sense tests have suggested that various categories of sportspersons have superior joint sense, 31,32 an unpublished study by the present authors found no significant difference in position sense accuracy or variability when active position sense tests results from 43 elite Australian Rules footballers were compared to the results from 16 age-matched control subjects (including 14 women). While a few studies have provided evidence of spinal proprioceptive adaptations to chronic exercise in experimental animals and sportspersons, 33 these adaptations are modest and involve an enhancement rather than a fundamental change in the pertinent peripheral and central neurobiology; therefore, it is likely that the neural mechanisms underpinning the present study are also present in the general population, but patients with various types of motor disorder from neurological dysfunction might not manifest the same kinesthetic response following strength testing or exercise. This difference, if there is one, is more likely to be related to a greater propensity to fatigue. It is postulated that patients with an intact nervous system are unlikely to manifest a fundamentally different kinesthetic response to nonfatiguing exercise. Until this matter is further clarified, it can only be recommended that clinicians be cautious about kinesthetic assessment shortly after a period of presumed nonfatiguing strength testing or exercise, and postpone kinesthetic tests following fatiguing contractions. In the present study both lower limbs were strength tested, and the order of limb testing was alternated during both the strength and joint sense tests; consequently, different periods of time elapsed between the offset of strength testing one limb, and the onset of position sense testing the same limb. Based on the average duration of the strength tests and position sense tests, the longest interval between strength test and position sense test of the same limb could have been 25min (eg, when the right (left) knee was strength tested first and position sense tested last). The shortest interval was less than 5min, therefore, it may be argued that in some limbs an acute potcontractional sensory effect may have been extinguished with time before the onset of position sense testing. Based on the present study one may argue 25min is the minimum time that may elapse between the offset strength testing and the onset of position sense tests without concern for contaminating postexercise effects. The subjects in this study all participated in a near-identical long-term fitness and skill training program, which caused the authors to conclude that their level of thigh muscle strength was both relatively similar and abnormally high. The strength testing program required each subject to perform maximum
AFTEREFFECTS OF EXERCISE ON JOINT SENSE, Stillman
voluntary contractions. This ensured that the difficulty level of the strength testing program was similar for all subjects. Moreover, as previously noted, the regime was not evidently taxing for any of the subjects. The general applicability of the experimental findings might conceivably be expanded by investigating the proprioceptive effects from different submaxireal levels of thigh muscle contractions; however the likelihood that nonfatiguing submaximal exercise regimes will interfere with subsequently tested joint position sense, when a maximum strength testing regime did not, seems remote. CONCLUSION The present study has shown that a regime of nonfatiguing nontraumatic maximally-resisted concentric and eccentric isokinetic quadriceps and hamstring contractions, occupying about 15rain per limb, had no statistically significant effect on either the accuracy (as evidenced by the relative and absolute errors) or precision (as evidenced by the variable errors) of knee joint position sense tested within 5 to 25rain of the offset of the strength tests. Since the presence and time course of postcontractional illusory effects remains to be fully elucidated, and in the present experiment there may have been hidden acute effects, it would be of value to extend the present study using only one lower limb so that the elapsed period before position sense testing could be systematically varied; for example, between 0 and 20rain. The findings from such a study might be enhanced by varying the number of repetitions in the exercise program to have nonfatigued, mildly fatigued, and markedly fatigued subgroups. Also, examination of different subject groups, including patients with broad-ranging disturbances of motor function, will be necessary to broaden the context of this area of investigation. It would also be of value both in sport and in rehabilitation medicine to clarify what forms of intervention can be used to extinguish the aftereffects of fatiguing exercise on joint sense. For example, joint sense disturbances following fatigue in sport might be a factor in precipitating sporting injuries. Are there simple strategies such as a period of unresisted reciprocal exercise--peddling a stationary bicycle, for example--that might be used to maintain or restore high levels of joint sense acuity following fatiguing exercise? The present study has added one additional piece of information to this emerging story of the relationship between exercise and kinesthetic acuity.
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Supplier a. Kinetic communicator (KIN-COM); Chattanooga Instruments, Inc., 101 Memorial Drive, Chattanooga, TN 37405.