Journal of Sport Rehabilitation, 2015, 24, 349 -352 http://dx.doi.org/10.1123/jsr.2014-0192 © 2015 Human Kinetics, Inc.
ORIGINAL RESEARCH REPORT
The Effect of Uphill and Downhill Walking on Joint-Position Sense: A Study on Healthy Knees Giuliamarta Bottoni, Dieter Heinrich, Philipp Kofler, Michael Hasler, and Werner Nachbauer Context: During sport activity, knee proprioception might worsen. This decrease in proprioceptive acuity negatively influences motor control and therefore may increase injury risk. Hiking is a common activity characterized by a higher-intensity-exercise phase during uphill walking and a lower-intensity-exercise phase during downhill walking. Pain and injuries are reported in hiking, especially during the downhill phase. Objective: To examine the effect of a hiking-fatigue protocol on joint-position sense. Design: Repeated measures. Setting: University research laboratory. Participants: 24 nonprofessional sportswomen without knee injuries. Main Outcome Measures: Joint-position sense was tested at the beginning, after 30 min uphill walking, and after 30 min downhill walking on a treadmill (continuous protocol). Results: After downhill walking, joint-position sense was significantly worse than in the test at the beginning (P = .035, α = .05). After uphill walking, no differences were observed in comparison with the test at the beginning (P = .172, α = .05) or the test after downhill walking (P = .165, α = .05). Conclusion: Downhill walking causes impairment in knee-joint-position sense. Considering these results, injury-prevention protocols for hiking should focus on maintaining and improving knee proprioception during the descending phase. Keywords: proprioception, hiking During hiking, pain and injuries are reported, especially during the downhill phase,1 and moreover the risk of falling and slipping is higher for downhill walking than for uphill or level walking.2,3 During downhill walking eccentric muscle contraction is needed to reduce the gain in kinetic energy due to descending during walking. 4 In other words, during downhill walking higher loads occur at the knee because there is the tendency to use eccentric force with short-muscle lengthening to control the downhill kinetic force.5,6 Of the injuries in hiking, 80% occur in the lower extremities, and of those, 19.2% occur at the knee.7 Proprioception is the capacity to feel the position of a joint in space, joint motion, and effort as sensed by the central nervous system.8 Fatigue or exercise-mediated alteration in proprioception might have a negative influence on motor control and increase injury risk.9–12 Proprioception is mediated by neural pathways from afferent receptors in the joint capsule, muscles, ligaments, and skin. It is assumed to have an important role in functional joint stability, and it allows the modulation of the stiffness of muscles that control the joint.9 Fatigue is defined as the transient inability to maintain power output during
Bottoni, Kofler, and Nachbauer are with the Dept of Sport Science, University of Innsbruck, Innsbruck, Austria. Heinrich and Hasler are with the Center of Technology of Ski and Alpine Sport, Innsbruck, Innsbruck, Austria. Address author correspondence to Giuliamarta Bottoni at [email protected].
repeated muscle contraction and can occur anywhere along the pathway involved in muscle contraction.9 It can be divided into central fatigue, which involves processes above the neuromuscular junction, and peripheral fatigue, which arises in the alpha motor neurons and involves the muscle and the contractile mechanism.9 The process that leads to fatigue varies depending on the type of exercise. Some evidence shows that loss of efficiency of muscle receptors, increased joint laxity, and metabolic acidosis resulting from muscle activity are related with deterioration in joint proprioception.10,13 Local fatigue of the lower extremities due to muscle exercise load and general tiredness due to activity might both contribute to injury risk because of an alteration of neuromuscular control. Skinner et al13 studied the effect of fatigue on the reproduction of knee-joint angles and on the threshold of detection of passive knee movement. After their subjects ran, they found a significant worsening of reproduction of knee-joint angles but not of threshold of detection of passive knee movement. Miura et al14 found an increase in the absolute error of reproduction of knee-joint angles after 5 minutes of running but not after a local load provided with maximum isokinetic knee flexion– extension. Ribeiro et al15 and Roberts et al16 found a reduction in joint-position sense after local exercise in elderly people and after 5 to 10 minutes of exhaustive cycling, respectively. Although many researchers have studied the effect of fatigue on knee proprioception it is still unclear which kind of fatigue process affects proprioception, and to the best of our knowledge, none has evaluated the effect of a hiking-fatigue protocol. 349
350 Bottoni et al
Hiking is a common activity characterized by a higher-intensity-exercise phase during uphill walking and a lower-intensity-exercise phase during downhill walking. The purpose of this study was to examine the effect of uphill and downhill walking on knee-joint-position sense. Both phases of hiking can induce a fatigue process able to alter proprioceptive acuity of the knee. Namely, during uphill walking fatigue might be caused by general exertion due to the energy costs and metabolic acidosis, while during downhill walking fatigue should be mainly produced by muscle damage due to eccentric exercise.4
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Methods Twenty-four female sport students took part in this study (mean ± SD age 23 ± 2.5 y, height 1.67 ± 0.06 m, mass 58 ± 5.3 kg). They took voluntary part in the study and were excluded if they reported a history of major hip, knee, or ankle injury or pathology or neurological diseases. All participants were nonprofessional sportswomen. No specifications about the practiced sport were required. The test procedure was approved by the institutional review board. The study took place in a climatic chamber (Kältepol, Natters—AT) at 25°C (50% humidity). This temperature and humidity were selected to simulate a typical summer climate. The subjects walked 30 minutes uphill at 20% inclination, 3 km/h, and 30 minutes downhill at 20% inclination, vdown =
2g l +1 p
where l is the leg length17, on a treadmill (Pulsar, h/p/ cosmos, Germany) wearing a T-shirt, sport shorts, short socks, and running shoes. Between uphill and downhill walking there was only a short break (about 3 min) to allow the proprioception test. Heart rate was continuously monitored with a heartrate monitor (Polar Electro Austria GmbH, Vienna, Austria) during the test. After uphill and downhill walking the subjective physical load was evaluated with a Borg scale of rating of perceived exertion, which ranges from 6 to 20, where 6 is no exertion and 20 is maximal exertion.18 At the beginning, after uphill walking, and after downhill walking, joint-position sense of the dominant leg was evaluated. The joint-position-sense measurement was validated by Beynnon et al.1 The dominant leg was determined as the leg used to kick a ball. The subject sat blindfolded to block visual input. From the starting position (90° knee angle) the leg was passively moved into extension by the examiner (about 5°/s) to a flexion angle between 30° and 70°. This target position was held for 5 seconds to allow the subject to memorize it and then the leg was returned by the examiner to the starting position. After a 5-second pause the subject had to actively repeat the preassessed position. The knee angle was recorded using 3 markers: 1 on the greater trochanter, 1 on lateral epicondyle of the femur, and 1 on the lateral
malleolus. The position of the markers was recorded with a camera (Exilim Pro EX-F1, Casio, Japan) positioned in the sagittal plane. From these data, the difference between the repeated (actively reproduced knee angle) and the target positions (passively positioned knee angle) was evaluated. Six repetitions were recorded and the mean of the differences was then used for the analysis. An overestimation, namely a repeated angle bigger than the target angle, corresponded to a positive error. An underestimation, namely a repeated angle smaller than the target angle, corresponded to a negative error. During the passive positioning of the leg, the subject had to keep the muscles as relaxed as possible. To familiarize them with the test methods, subjects had 5 to 10 practice trials before the start of the test. Coordinates of the markers were digitized using LabVIEW 2010 example code “Optical Flow Feature Tracking Example.” Target and repeated angles were subsequently computed in MATLAB 2009. As proposed by Ribeiro et al,15 proprioception was evaluated by measuring the absolute angular error (defined as the absolute difference between the repeated and the target position), the relative angular error (defined as the arithmetic difference between the 2 positions), and the variable angular error (standard deviation from the mean of the relative errors). All data were analyzed with the statistical software SPSS 18.0 (SPSS Inc, Chicago). A 1-way analysis of variance (ANOVA) with repeated measures was used to analyze the effect of uphill and downhill walking on joint-position sense. Post hoc tests were computed with Bonferroni adjustment. The level of significance was set at P = .05.
Results The average heart rate at the start was 95 ± 9 beats/min, after 30 minutes uphill walking was 163 ± 16 beats/ min, and after 30 minutes downhill walking was 122 ± 17 beats/min. The average subjective fatigue measured with the Borg scale was 13.2 ± 1.7 (somewhat hard) after 30 minutes uphill walking and 11 ± 1.6 (fairly light/ somewhat hard) after downhill walking. Both the repositioning absolute error and relative error exhibited a variation between the repetitions at the beginning, after uphill walking, and after downhill walking (P = .013 and P < .001) (Table 1). The absolute error significantly increased after downhill walking, in comparison with the results at the beginning (P = .035). After uphill walking no differences were observed in comparison with either the test at the beginning (P = .172) or the test after downhill walking (P = .165). The subjects tended to overestimate their joint position. The relative error showed that this overestimation was significantly higher after downhill walking than at the beginning (P = .002) and after uphill walking (P = .007). No differences in the relative error could be seen from the beginning to the test after uphill walking (P = .785).
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A Proprioception Study on Uninjured Knees 351
Table 1 Effects of Walking-Induced Fatigue on Joint-Position Sense of the Knee (Mean ± SD), N = 24 Error, °
Beginning
Postuphill
Postdownhill
Mean
3.54 ± 1.63
4.09 ± 1.79
5.02 ± 2.84*
Relative
2.11 ± 2.49
2.61 ± 2.73
4.10 ± 2.75*†
Variable
2.48 ± 1.56
2.73 ± 2.43
2.75 ± 3.15
*Significantly different from beginning, P < .05. †Significantly different from postuphill, P < .05.
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The reliability and accuracy in estimating knee angle, expressed by variable error, did not change during the test (P = .674).
Discussion The aim of this study was to investigate the effect of uphill and downhill walking on knee-joint-position sense. The average absolute error values of joint-position sense of this study were similar to the values reported in other studies,13,14 suggesting the reliability of the test method. In the study of Miura et al14 the error in reproduction of knee-joint angle was between 3.38° and 5.10°, while Skinner et al13 found values between 1.9° and 4.8°. These results are similar to the values found in this study, which lay between 3.54° and 5.02°. The main finding of this study was a significant decrease in joint-position sense after 30 minutes uphill and 30 minutes downhill walking. This is in agreement with the findings of previous studies that showed a decrease in knee-joint-position reproduction accuracy after exercise.10,13-15,19 However, considering just the first 30 minutes uphill walking at 3 km/h and 20% inclination, joint-position sense did not significantly differ from the test at the beginning. The joint-position-sense relative error showed that the subjects generally overestimated the target joint position in all test repetitions, and this overestimation became worse after uphill and after downhill walking. As explained by Riberio et al,15 this increased overestimation after activity might be connected with a sensory illusion of increased flexion in the initial position caused by a persisting contraction of intrafusal fibers of the muscle spindles in previously contracted muscles. Other authors have evaluated the effect of activity on knee proprioception. Miura et al14 and Skinner et al13 used a running protocol and found a significant worsening in the absolute error in joint reproduction. Miura et al14 compared the effect of local concentric load and general load on joint-position sense and found a significant increase in the angle-reproduction error after general load. Those authors concluded that general load decreases joint proprioception because of a negative effect of general fatigue on the proprioceptive pathway and on proprioceptive-signal processing. Skinner et al13 concluded that muscle receptors have a prominent role in joint-position sense and connected
the worsening they found after the fatigue protocol to a loss of efficiency of these receptors. In other studies, however, a worsening in joint-position sense after local load is reported. 20,15,19 Marks19 and Ju et al 20 used, respectively, 20 and 60 isokinetic maximum concentric and eccentric contractions. The findings of those 2 studies in combination with the results of the current study might contradict the conclusion of Miura et al14 and shift the cause of the decrease in joint-position sense from a general fatigue process to the load in the lower-extremity muscles due to eccentric contractions. Two main types of muscle fatigue are induced by exercise: metabolic and nonmetabolic fatigue.21 Metabolic fatigue is related to a failure in maintaining the desired ATP production rates and the accumulation of metabolic-reactions products; nonmetabolic fatigue is caused by internal muscle stress, which is associated with a damage of internal muscle structures. Although muscle fatigue was not measured in the current study, based on the perceived exertion measured with the Borg scale we can assume that a fatiguing process was initialized and the subjects were more exhausted after uphill walking than after downhill walking. A higher general fatigue level can be supposed after uphill walking than after downhill walking, as confirmed also by the heart-rate data. During uphill walking the lower-extremity muscles act concentrically and the fatigue process is mainly due to the accumulation of metabolic-reaction products.4 During the following 30 minutes of downhill walking the fatigue process should mainly be produced by muscle-fiber damages.4 In the study of Miura et al14 the subjects ran 5 minutes at 10 km/h and 10% uphill grade. The energy requirement for this activity can be approximated as ~60 kcal. This energy requirement is lower than the energy requirement for the uphill phase of the current study, for which ~145 kcal can be estimated using the classification of Ainsworth et al.22 If the decrease in proprioception found by Miura et al14 were caused by general fatigue, the same results should be found in the current study. Downhill walking in the current study, running,1,14 and knee flexion/ extension19,20 all include eccentric loading of the knee-joint muscles. Therefore, we conclude that the worsening in jointposition sense found in this study was caused by damage to the muscle fibers due to eccentric exercise. This damage influences the activity of the muscle mechanoreceptors, which are directly involved in proprioception, as suggested by Clark et al23 and Skinner et al.13 Muscle damage alters lactic acid concentration, temperature, and pH; all these factors might contribute to a loss in efficiency of the muscle receptors involved in knee-joint-position sense. An influence of general fatigue due to prolonged activity on joint proprioception, as suggested by Miura et al,14 should not be completely excluded. As those authors suggested, general fatigue might affect the central processing of proprioceptive signals. It is known that tiredness causes a reduction in movement control, which might enhance injury risk,9,10,12 and this reduction in movement control may be connected with a decrease in proprioceptive ability.
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352 Bottoni et al
Some limitations have to be considered for the current study. First of all, the walking protocol was shorter than a normal hiking excursion. Second, the subjects walked at a constant incline and on even surface on a treadmill, but during hiking the inclination normally varies and the ground is irregular. Third, the training level of the subjects should have been included in the analysis. Knee proprioception of people used to hiking and with a higher training level is, indeed, supposed to be less affected by the protocol used in this study. For the analysis it would have been better to separate the subjects based on their training level. Further studies in which the eccentric fatigue activity is isolated and muscle fatigue is measured parallel to proprioception are needed to better understand the effect of exercise and a fatiguing process on knee proprioception.
Conclusion Knee-joint-position sense of healthy trained subjects significantly worsened after 30 minutes of uphill walking followed by 30 minutes of downhill walking. The greater worsening manifested during the downhill phase. Considering these results, injury-prevention protocols for hiking should focus on maintaining and improving knee proprioception during the descending phase.
References 1. Beynnon BD, Renström PA, Konradsen L, Elmqvist LG, Gottlieb D, Dirks M. Validation of techniques to measure knee proprioception. In: Lephart SM, Fu FH, eds. Proprioception and Neuromuscular Control in Joint Stability. Champaign, IL: Human Kinetics; 2000:127–138. 2. Redfern MS, DiPasquale J. Biomechanics of descending ramps. Gait Posture. 1997;6(2):119–125. doi:10.1016/ S0966-6362(97)01117-X 3. Sheehan RC, Gottschall JS. Preferred step frequency during downhill running may be determined by muscle activity. J Electromyogr Kinesiol. 2013;23(4):826–830. PubMed doi:10.1016/j.jelekin.2013.03.013 4. Chapman AE. Biomechanical Analysis of Fundamental Human Movements. Champaign, IL: Human Kinetics; 2008. 5. Kuster M, Sakurai S, Wood GA. Kinematic and kinetic comparison of downhill and level walking. Clin Biomech (Bristol, Avon). 1995;10(2):79–84. PubMed doi:10.1016/0268-0033(95)92043-L 6. Schwameder H, Roithner R, Müller E, Niessen W, Raschner C. Knee joint forces during downhill walking with hiking poles. J Sports Sci. 1999;17:969–978. PubMed doi:10.1080/026404199365362 7. Blake RL, Ferguson HJ. Walking and hiking injuries: a one year follow-up study. J Am Podiatr Med Assoc. 1993;83(9):499–503. PubMed doi:10.7547/8750731583-9-499 8. Lephart SM, Riemann BL, Fu FH. Introduction of the sensorimotor system. In: Lephart SM, Fu FH, eds.
Proprioception and Neuromuscular Control in Joint Stability. Champaign, IL: Human Kinetics; 2000:xvii– xxiv. 9. Hiemstra LA, Lo IKY, Fowler PJ. Effect of fatigue on knee proprioception: implications for dynamic stabilization. J Orthop Sports Phys Ther. 2001;31(10):598–605. PubMed doi:10.2519/jospt.2001.31.10.598 10. Johnston RB, Howard ME, Cawley PW, Losse GM. Effect of lower extremity fatigue on motor control performance. Med Sci Sports Exerc. 1998;30(12):1703–1707. PubMed doi:10.1097/00005768-199812000-00008 11. Koller A, Sumann G, Schobersberger W, Hosertnagl H, Haid C. Decrease in eccentric hamstring strength in runners in the Tirol Speed Marathon. Br J Sports Med. 2006;40:850– 852. PubMed doi:10.1136/bjsm.2006.028175 12. Wojtys EM, Wylie BB, Huston LJ. The effects of muscle fatigue on neuromuscular function and anterior tibial translation in healthy knees. Am J Sports Med. 1996;24(5):615–621. PubMed doi:10.1177/036354659602400509 13. Skinner HB, Wyatt MP, Hodgdon JA, Conrad DW, Barrack RL. Effect of fatigue on joint position sense of the knee. J Orthop Res. 1986;4:112–118. PubMed doi:10.1002/ jor.1100040115 14. Miura K, Ishibashi Y, Tsuda E, Okamura Y, Otsuka H, Toh S. The effect of local and general fatigue on knee proprioception. Arthroscopy. 2004;20(4):414–418. PubMed doi:10.1016/j.arthro.2004.01.007 15. Ribeiro F, Oliveira MJ. Effect of exercise-induced fatigue on position sense of the knee in the elderly. Eur J Appl Physiol. 2007;99:379–385. PubMed doi:10.1007/s00421006-0357-8 16. Roberts D, Ageberg E, Andersson G, Fridén T. Effects of short-term cycling on knee joint proprioception in healthy young persons. Am J Sports Med. 2003;31(6):990–994. PubMed 17. Rodewald B, Schlichting H. Springen, gehen, laufen. Prax Natwiss Phys. 1988;37(5):12–14. 18. Borg G. Borg’s Perceived Exertion and Pain Scales. Champaign, IL: Human Kinetics; 1998. 19. Marks R. Effects of exercise-induced fatigue on position sense of the knee. Aust J Physiother. 1994;40(3):175–181. PubMed doi:10.1016/S0004-9514(14)60576-6 20. Ju YY, Wang CW, Cheng HYK. Effects of active fatiguing movements versus passive repetitive movement on knee proprioception. Clin Biomech (Bristol, Avon). 2010;25:708–712. PubMed doi:10.1016/j. clinbiomech.2010.04.017 21. Green HJ. Mechanisms of muscle fatigue in intense exercise. J Sports Sci. 1997;15:247–256. PubMed doi:10.1080/026404197367254 22. Ainsworth BE, Haskell WL, Leon AS, et al. Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc. 1993;25(1):71–80. PubMed doi:10.1249/00005768199301000-00011 23. Clark FJ, Burgess RC, Chapin JW, Lipscomb WT. Role of intramuscular receptor in the awareness of limb position. J Neurophysiol. 1985;54(6):1529–1540. PubMed
JSR Vol. 24, No. 4, 2015
ORIGINAL RESEARCH REPORT
The Effect of Uphill and Downhill Walking on Joint-Position Sense: A Study on Healthy Knees Giuliamarta Bottoni, Dieter Heinrich, Philipp Kofler, Michael Hasler, and Werner Nachbauer Context: During sport activity, knee proprioception might worsen. This decrease in proprioceptive acuity negatively influences motor control and therefore may increase injury risk. Hiking is a common activity characterized by a higher-intensity-exercise phase during uphill walking and a lower-intensity-exercise phase during downhill walking. Pain and injuries are reported in hiking, especially during the downhill phase. Objective: To examine the effect of a hiking-fatigue protocol on joint-position sense. Design: Repeated measures. Setting: University research laboratory. Participants: 24 nonprofessional sportswomen without knee injuries. Main Outcome Measures: Joint-position sense was tested at the beginning, after 30 min uphill walking, and after 30 min downhill walking on a treadmill (continuous protocol). Results: After downhill walking, joint-position sense was significantly worse than in the test at the beginning (P = .035, α = .05). After uphill walking, no differences were observed in comparison with the test at the beginning (P = .172, α = .05) or the test after downhill walking (P = .165, α = .05). Conclusion: Downhill walking causes impairment in knee-joint-position sense. Considering these results, injury-prevention protocols for hiking should focus on maintaining and improving knee proprioception during the descending phase. Keywords: proprioception, hiking During hiking, pain and injuries are reported, especially during the downhill phase,1 and moreover the risk of falling and slipping is higher for downhill walking than for uphill or level walking.2,3 During downhill walking eccentric muscle contraction is needed to reduce the gain in kinetic energy due to descending during walking. 4 In other words, during downhill walking higher loads occur at the knee because there is the tendency to use eccentric force with short-muscle lengthening to control the downhill kinetic force.5,6 Of the injuries in hiking, 80% occur in the lower extremities, and of those, 19.2% occur at the knee.7 Proprioception is the capacity to feel the position of a joint in space, joint motion, and effort as sensed by the central nervous system.8 Fatigue or exercise-mediated alteration in proprioception might have a negative influence on motor control and increase injury risk.9–12 Proprioception is mediated by neural pathways from afferent receptors in the joint capsule, muscles, ligaments, and skin. It is assumed to have an important role in functional joint stability, and it allows the modulation of the stiffness of muscles that control the joint.9 Fatigue is defined as the transient inability to maintain power output during
Bottoni, Kofler, and Nachbauer are with the Dept of Sport Science, University of Innsbruck, Innsbruck, Austria. Heinrich and Hasler are with the Center of Technology of Ski and Alpine Sport, Innsbruck, Innsbruck, Austria. Address author correspondence to Giuliamarta Bottoni at [email protected].
repeated muscle contraction and can occur anywhere along the pathway involved in muscle contraction.9 It can be divided into central fatigue, which involves processes above the neuromuscular junction, and peripheral fatigue, which arises in the alpha motor neurons and involves the muscle and the contractile mechanism.9 The process that leads to fatigue varies depending on the type of exercise. Some evidence shows that loss of efficiency of muscle receptors, increased joint laxity, and metabolic acidosis resulting from muscle activity are related with deterioration in joint proprioception.10,13 Local fatigue of the lower extremities due to muscle exercise load and general tiredness due to activity might both contribute to injury risk because of an alteration of neuromuscular control. Skinner et al13 studied the effect of fatigue on the reproduction of knee-joint angles and on the threshold of detection of passive knee movement. After their subjects ran, they found a significant worsening of reproduction of knee-joint angles but not of threshold of detection of passive knee movement. Miura et al14 found an increase in the absolute error of reproduction of knee-joint angles after 5 minutes of running but not after a local load provided with maximum isokinetic knee flexion– extension. Ribeiro et al15 and Roberts et al16 found a reduction in joint-position sense after local exercise in elderly people and after 5 to 10 minutes of exhaustive cycling, respectively. Although many researchers have studied the effect of fatigue on knee proprioception it is still unclear which kind of fatigue process affects proprioception, and to the best of our knowledge, none has evaluated the effect of a hiking-fatigue protocol. 349
350 Bottoni et al
Hiking is a common activity characterized by a higher-intensity-exercise phase during uphill walking and a lower-intensity-exercise phase during downhill walking. The purpose of this study was to examine the effect of uphill and downhill walking on knee-joint-position sense. Both phases of hiking can induce a fatigue process able to alter proprioceptive acuity of the knee. Namely, during uphill walking fatigue might be caused by general exertion due to the energy costs and metabolic acidosis, while during downhill walking fatigue should be mainly produced by muscle damage due to eccentric exercise.4
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Methods Twenty-four female sport students took part in this study (mean ± SD age 23 ± 2.5 y, height 1.67 ± 0.06 m, mass 58 ± 5.3 kg). They took voluntary part in the study and were excluded if they reported a history of major hip, knee, or ankle injury or pathology or neurological diseases. All participants were nonprofessional sportswomen. No specifications about the practiced sport were required. The test procedure was approved by the institutional review board. The study took place in a climatic chamber (Kältepol, Natters—AT) at 25°C (50% humidity). This temperature and humidity were selected to simulate a typical summer climate. The subjects walked 30 minutes uphill at 20% inclination, 3 km/h, and 30 minutes downhill at 20% inclination, vdown =
2g l +1 p
where l is the leg length17, on a treadmill (Pulsar, h/p/ cosmos, Germany) wearing a T-shirt, sport shorts, short socks, and running shoes. Between uphill and downhill walking there was only a short break (about 3 min) to allow the proprioception test. Heart rate was continuously monitored with a heartrate monitor (Polar Electro Austria GmbH, Vienna, Austria) during the test. After uphill and downhill walking the subjective physical load was evaluated with a Borg scale of rating of perceived exertion, which ranges from 6 to 20, where 6 is no exertion and 20 is maximal exertion.18 At the beginning, after uphill walking, and after downhill walking, joint-position sense of the dominant leg was evaluated. The joint-position-sense measurement was validated by Beynnon et al.1 The dominant leg was determined as the leg used to kick a ball. The subject sat blindfolded to block visual input. From the starting position (90° knee angle) the leg was passively moved into extension by the examiner (about 5°/s) to a flexion angle between 30° and 70°. This target position was held for 5 seconds to allow the subject to memorize it and then the leg was returned by the examiner to the starting position. After a 5-second pause the subject had to actively repeat the preassessed position. The knee angle was recorded using 3 markers: 1 on the greater trochanter, 1 on lateral epicondyle of the femur, and 1 on the lateral
malleolus. The position of the markers was recorded with a camera (Exilim Pro EX-F1, Casio, Japan) positioned in the sagittal plane. From these data, the difference between the repeated (actively reproduced knee angle) and the target positions (passively positioned knee angle) was evaluated. Six repetitions were recorded and the mean of the differences was then used for the analysis. An overestimation, namely a repeated angle bigger than the target angle, corresponded to a positive error. An underestimation, namely a repeated angle smaller than the target angle, corresponded to a negative error. During the passive positioning of the leg, the subject had to keep the muscles as relaxed as possible. To familiarize them with the test methods, subjects had 5 to 10 practice trials before the start of the test. Coordinates of the markers were digitized using LabVIEW 2010 example code “Optical Flow Feature Tracking Example.” Target and repeated angles were subsequently computed in MATLAB 2009. As proposed by Ribeiro et al,15 proprioception was evaluated by measuring the absolute angular error (defined as the absolute difference between the repeated and the target position), the relative angular error (defined as the arithmetic difference between the 2 positions), and the variable angular error (standard deviation from the mean of the relative errors). All data were analyzed with the statistical software SPSS 18.0 (SPSS Inc, Chicago). A 1-way analysis of variance (ANOVA) with repeated measures was used to analyze the effect of uphill and downhill walking on joint-position sense. Post hoc tests were computed with Bonferroni adjustment. The level of significance was set at P = .05.
Results The average heart rate at the start was 95 ± 9 beats/min, after 30 minutes uphill walking was 163 ± 16 beats/ min, and after 30 minutes downhill walking was 122 ± 17 beats/min. The average subjective fatigue measured with the Borg scale was 13.2 ± 1.7 (somewhat hard) after 30 minutes uphill walking and 11 ± 1.6 (fairly light/ somewhat hard) after downhill walking. Both the repositioning absolute error and relative error exhibited a variation between the repetitions at the beginning, after uphill walking, and after downhill walking (P = .013 and P < .001) (Table 1). The absolute error significantly increased after downhill walking, in comparison with the results at the beginning (P = .035). After uphill walking no differences were observed in comparison with either the test at the beginning (P = .172) or the test after downhill walking (P = .165). The subjects tended to overestimate their joint position. The relative error showed that this overestimation was significantly higher after downhill walking than at the beginning (P = .002) and after uphill walking (P = .007). No differences in the relative error could be seen from the beginning to the test after uphill walking (P = .785).
JSR Vol. 24, No. 4, 2015
A Proprioception Study on Uninjured Knees 351
Table 1 Effects of Walking-Induced Fatigue on Joint-Position Sense of the Knee (Mean ± SD), N = 24 Error, °
Beginning
Postuphill
Postdownhill
Mean
3.54 ± 1.63
4.09 ± 1.79
5.02 ± 2.84*
Relative
2.11 ± 2.49
2.61 ± 2.73
4.10 ± 2.75*†
Variable
2.48 ± 1.56
2.73 ± 2.43
2.75 ± 3.15
*Significantly different from beginning, P < .05. †Significantly different from postuphill, P < .05.
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The reliability and accuracy in estimating knee angle, expressed by variable error, did not change during the test (P = .674).
Discussion The aim of this study was to investigate the effect of uphill and downhill walking on knee-joint-position sense. The average absolute error values of joint-position sense of this study were similar to the values reported in other studies,13,14 suggesting the reliability of the test method. In the study of Miura et al14 the error in reproduction of knee-joint angle was between 3.38° and 5.10°, while Skinner et al13 found values between 1.9° and 4.8°. These results are similar to the values found in this study, which lay between 3.54° and 5.02°. The main finding of this study was a significant decrease in joint-position sense after 30 minutes uphill and 30 minutes downhill walking. This is in agreement with the findings of previous studies that showed a decrease in knee-joint-position reproduction accuracy after exercise.10,13-15,19 However, considering just the first 30 minutes uphill walking at 3 km/h and 20% inclination, joint-position sense did not significantly differ from the test at the beginning. The joint-position-sense relative error showed that the subjects generally overestimated the target joint position in all test repetitions, and this overestimation became worse after uphill and after downhill walking. As explained by Riberio et al,15 this increased overestimation after activity might be connected with a sensory illusion of increased flexion in the initial position caused by a persisting contraction of intrafusal fibers of the muscle spindles in previously contracted muscles. Other authors have evaluated the effect of activity on knee proprioception. Miura et al14 and Skinner et al13 used a running protocol and found a significant worsening in the absolute error in joint reproduction. Miura et al14 compared the effect of local concentric load and general load on joint-position sense and found a significant increase in the angle-reproduction error after general load. Those authors concluded that general load decreases joint proprioception because of a negative effect of general fatigue on the proprioceptive pathway and on proprioceptive-signal processing. Skinner et al13 concluded that muscle receptors have a prominent role in joint-position sense and connected
the worsening they found after the fatigue protocol to a loss of efficiency of these receptors. In other studies, however, a worsening in joint-position sense after local load is reported. 20,15,19 Marks19 and Ju et al 20 used, respectively, 20 and 60 isokinetic maximum concentric and eccentric contractions. The findings of those 2 studies in combination with the results of the current study might contradict the conclusion of Miura et al14 and shift the cause of the decrease in joint-position sense from a general fatigue process to the load in the lower-extremity muscles due to eccentric contractions. Two main types of muscle fatigue are induced by exercise: metabolic and nonmetabolic fatigue.21 Metabolic fatigue is related to a failure in maintaining the desired ATP production rates and the accumulation of metabolic-reactions products; nonmetabolic fatigue is caused by internal muscle stress, which is associated with a damage of internal muscle structures. Although muscle fatigue was not measured in the current study, based on the perceived exertion measured with the Borg scale we can assume that a fatiguing process was initialized and the subjects were more exhausted after uphill walking than after downhill walking. A higher general fatigue level can be supposed after uphill walking than after downhill walking, as confirmed also by the heart-rate data. During uphill walking the lower-extremity muscles act concentrically and the fatigue process is mainly due to the accumulation of metabolic-reaction products.4 During the following 30 minutes of downhill walking the fatigue process should mainly be produced by muscle-fiber damages.4 In the study of Miura et al14 the subjects ran 5 minutes at 10 km/h and 10% uphill grade. The energy requirement for this activity can be approximated as ~60 kcal. This energy requirement is lower than the energy requirement for the uphill phase of the current study, for which ~145 kcal can be estimated using the classification of Ainsworth et al.22 If the decrease in proprioception found by Miura et al14 were caused by general fatigue, the same results should be found in the current study. Downhill walking in the current study, running,1,14 and knee flexion/ extension19,20 all include eccentric loading of the knee-joint muscles. Therefore, we conclude that the worsening in jointposition sense found in this study was caused by damage to the muscle fibers due to eccentric exercise. This damage influences the activity of the muscle mechanoreceptors, which are directly involved in proprioception, as suggested by Clark et al23 and Skinner et al.13 Muscle damage alters lactic acid concentration, temperature, and pH; all these factors might contribute to a loss in efficiency of the muscle receptors involved in knee-joint-position sense. An influence of general fatigue due to prolonged activity on joint proprioception, as suggested by Miura et al,14 should not be completely excluded. As those authors suggested, general fatigue might affect the central processing of proprioceptive signals. It is known that tiredness causes a reduction in movement control, which might enhance injury risk,9,10,12 and this reduction in movement control may be connected with a decrease in proprioceptive ability.
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352 Bottoni et al
Some limitations have to be considered for the current study. First of all, the walking protocol was shorter than a normal hiking excursion. Second, the subjects walked at a constant incline and on even surface on a treadmill, but during hiking the inclination normally varies and the ground is irregular. Third, the training level of the subjects should have been included in the analysis. Knee proprioception of people used to hiking and with a higher training level is, indeed, supposed to be less affected by the protocol used in this study. For the analysis it would have been better to separate the subjects based on their training level. Further studies in which the eccentric fatigue activity is isolated and muscle fatigue is measured parallel to proprioception are needed to better understand the effect of exercise and a fatiguing process on knee proprioception.
Conclusion Knee-joint-position sense of healthy trained subjects significantly worsened after 30 minutes of uphill walking followed by 30 minutes of downhill walking. The greater worsening manifested during the downhill phase. Considering these results, injury-prevention protocols for hiking should focus on maintaining and improving knee proprioception during the descending phase.
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