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Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue
THEKNE-01987; No of Pages 6 The Knee xxx (2015) xxx–xxx
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The Knee
Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue Eduardo Salgado a, Fernando Ribeiro b, José Oliveira a,⁎ a b
University of Porto, Faculty of Sport, Research Centre in Physical Activity, Health and Leisure (CIAFEL), Porto, Portugal School of Health Sciences, University of Aveiro, Aveiro, Portugal
a r t i c l e
i n f o
Article history: Received 3 February 2014 Received in revised form 7 July 2014 Accepted 13 October 2014 Available online xxxx Keywords: Football Proprioception Warm-up Fatigue
a b s t r a c t Background: The demands to which football players are exposed during the match may augment the risk of injury by decreasing the sense of joint position. This study aimed to assess the effect of pre-participation warm-up and fatigue induced by an official football match on the knee-joint-position sense of football players. Methods: Fourteen semi-professional male football players (mean age: 25.9 ± 4.6 years old) volunteered in this study. The main outcome measures were rate of perceived exertion and knee-joint-position sense assessed at rest, immediately after a standard warm-up (duration 25 min), and immediately after a competitive football match (90 minutes duration). Results: Perceived exertion increased significantly from rest to the other assessments (rest: 8.6 ± 2.0; after warm-up: 12.1 ± 2.1; after football match: 18.5 ± 1.3; p b 0.001). Compared to rest, absolute angular error decreased significantly after the warm-up (4.1° ± 2.2° vs. 2.0° ± 1.0°; p = 0.0045). After the match, absolute angular error (8.7° ± 3.8°) increased significantly comparatively to both rest (p = 0.001) and the end of warm-up (p b 0.001). Relative error showed directional bias with an underestimation of the target position, which was higher after the football match compared to both rest (p b 0.001) and after warm-up (p b 0.001). Conclusions: The results indicate that knee-joint-position sense acuity was increased by pre-participation warm-up exercise and was decreased by football match-induced fatigue. Clinical relevance: Warm-up exercises could contribute to knee injury prevention, whereas the deleterious effect of match-induced fatigue on the sensorimotor system could ultimately contribute to knee instability and injury. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Proprioception contributes to several conscious and unconscious sensations, automatic control of movement, balance and postural control, and joint stability, as a result of neural cumulative input to the central nervous system proceeding from specialized nerve endings called mechanoreceptors [1,2]. Joint position sense (JPS), a sub-modality of proprioception, is generally defined as the awareness of the joint position and represents the ability to identify and reproduce a joint angle after the limb has been moved [1]. In sports activities, like football, joint position sense acuity could be paramount for overall performance, since it is related with the level of skills accuracy [2] and the risk of injury [3]. Indeed, changes in the state of the muscle induced by moderate-intensity, warm-up exercise, or muscle fatigue induced by high-intensity exercise could have repercussions on the muscular receptors, which are described as the main sources of afferent information contributing to joint-position sense [4, ⁎ Corresponding author at: Research Centre in Physical Activity, Health and Leisure (CIAFEL), Faculty of Sport, University of Porto, Rua Dr. Plácido Costa, 91, 4200-450 Porto, Portugal. Tel.: +351 22 5074773; fax: +351 22 5500689. E-mail address: [email protected] (J. Oliveira).
5]. However, the repercussions of exercise-induced fatigue on muscle receptors are controversial, as there are studies in cats showing that fatiguing eccentric muscle contractions have no repercussions on the muscle receptors [6,7]. Warm-up exercises are recognized to have positive effects on performance by reducing muscle stiffness, ameliorating the viscoelastic function of structures surrounding the joints, and increasing neural conduction and velocity, and metabolic efficiency [8,9]. However, only few studies [10–13] have been conducted evaluating the effect of warm-up on proprioception. Despite using different warm-up protocols and different methods to measure proprioception, these studies reported positive effects on knee proprioception after warm-up. On the other hand, high intensity exercise is associated with the reduction of muscle force, joint range of motion, and joint stability. It is also associated with clumsiness in movements demanding high levels of accuracy [14–17]. Several studies have shown that immediately after strenuous exercise, the size of the errors observed during positionmatching tasks increases significantly [18–20]. Investigations targeting the effects of mild intensity warm-up exercise and exercise-induced muscle fatigue on joint-position sense acuity have rarely been conducted in athletes. Additionally, the exercise protocols commonly used do not mimic the specific demands of
http://dx.doi.org/10.1016/j.knee.2014.10.002 0968-0160/© 2015 Elsevier B.V. All rights reserved.
Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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sporting activities. To our knowledge, few studies [18,21] assessed changes in proprioception induced by sporting activities. It is established that pre-participation warm-up improves physical performance [9], which could be explained, at least partially, by the improvement of sense of limb position. Conversely, the prolonged duration and intense muscle demands to which football players are exposed during the match might have deleterious effects on knee-joint-position sense, hence decreasing the sense of limb position, increasing errors, and augmenting the risk of injury [3]. Thus, the purpose of the present study was to assess the effect of pre-participation warm-up and fatigue induced by an official football match on knee-joint-position sense in football players. We hypothesize that pre-participation warm-up will improve knee position sense, whereas the football match will reduce knee position sense to values below those observed at rest. In this sense, if our hypothesis is confirmed, it will reinforce the importance of warming-up before a football match and reinforce the need to improve strategies to attenuate the impact of fatigue on joint proprioception in order to decrease the risk of injuries. 2. Methods 2.1. Participants and study design Fourteen healthy adult male semi-professional football players volunteered to participate in this study (mean age: 25.9 ± 4.6 years old, mean height: 179 ± 5 cm, mean weight: 75.4 ± 3.5 kg). The statistical power for the matched pairs analysis was computed a priori to establish the necessary sample size to achieve 95% power with α = 5% to detect differences in absolute angular error between the baseline and post-warm-up or post-match. This calculation was performed based on data presented in previous studies, respectively for baseline– warm-up [10] and baseline–end of the match [18]. It revealed that 14 participants were required (including a possible drop-out rate of three participants). Participants were volunteers recruited from a semi-professional football team. To be included in the study, participants had to have practiced football for more than 8 years (to minimize any possible influence of training and competitive experience on jointposition sense) with a frequency of at least three times per week and a normal knee range of motion. Participants were excluded according to the following criteria: lower limb or lower back injury in the 6 months before the study, history of knee surgery, taking medication with an influence on motor control and/or attention, and vestibular or neuromuscular disorders. Appropriate ethical approval from our institutional board was granted prior to the commencement of the study. All participants provided written, informed consent, and all procedures were conducted according the declaration of Helsinki. The study design is depicted in Fig. 1. In brief, the recruitment and selection of the participants was performed 1 month before starting data collection. The rate of perceived exertion (RPE) [22] and knee-joint-position sense were measured at rest, immediately after a standard warm-up (duration 25 min) and immediately after a competitive football match (approximate time slot of 90 min plus, on average, 4 min of extra time due to stoppages). Due to the time required to assess joint-position sense and in order to avoid the disappearance of the acute effects of both the warm-up and match on joint-position sense, only two players were evaluated in each game. Additionally, since the games where the data was collected were official competitive games, the time between warm-up and the start of the game was very small, thus leaving little room for the joint-position sense assessment. As a result, a total of seven competitive games, from February to April, were covered to collect data from 14 players. 2.2. Evaluation of rate of perceived exertion The evaluation of the rate of perceived exertion (RPE) was performed using Borg's rating-of-perceived-exertion scale (scale of 6 to
Fig. 1. Study timeline and design.
20 points) [22]. The RPE scale was used to evaluate the exercise intensity during the warm-up and the football match. Participants were considered to be fatigued if they reported an RPE of 15 or above [23,24]. Indeed, a score of 15 was reported as being strongly correlated with the metabolic responses of fatigue [25]. 2.3. Evaluation of joint-position sense Knee-joint-position sense of the dominant limb was evaluated using a technique of open-kinetic chain and active knee positioning of a passively determined position [26]. The technique was ipsilateral and performed without visual input [26]. The dominant limb was determined by asking which lower limb they normally use to shoot, pass and tackle. The dominant limb was the right lower limb in all the participants. The same examiner conducted all the procedures. Additionally, the matches were always on Sundays at 3 p.m. Prior to the joint-position-sense assessment, four reflective markers were fixed with double-sided adhesive tape to the skin of the apex of the greater trochanter; the iliotibial tract, level with the posterior crease of the knee when flexed to 80°; the head of the fibula; and the prominence of the lateral malleolus [26,27]. Since the markers were removed after each evaluation, their places were marked on the skin to avoid differences among evaluations. Each pair of markers represents the axis of the thigh and the leg. To record the joint positions, a tripodmounted video camera was used. It was positioned 7 m away from the participant – at the same level as the knee joint – and then manually focused on the field of view. The camera was in the sagittal plane. The same video camera was used over the experimental period. Natural vertical and horizontal lines in the videotaped environment were aligned parallel to the horizontal and vertical edges of the viewfinder to minimize camera tilt. To evaluate joint-position sense, participants, wearing shorts, were seated on a physiotherapy treatment table with their legs hanging freely but not touching the ground, and were blindfolded to remove visual input. To avoid verbal-sound cues, all the evaluations took place in a
Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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silent room, and only the examined athlete and the investigator were inside. The starting position was 90° of knee flexion and the repositioning movement was into knee extension. The examiner slowly (at approximately 10°/s) moved the leg from the starting position (90° of knee flexion) to a random knee angle between 40° and 60° of flexion. Then, the subject maintained the test position actively for 5 s in order to identify (memorize) that position. After that, the subject was instructed by the examiner to actively return the leg to the starting position and to immediately extend the knee actively in an attempt (upon the command “reposition”) to reproduce the test position using the same limb. The subject then returned to the position perceived as the test position and reported “target” to the examiner. This position was held for 5 s, and on the command “return,” the subject returned to the initial position and repeated the repositioning twice. Thus, subjects performed three repetitions (actively reproduced knee angle) in order to reproduce one target angle (passively positioned knee angle). The participants were told to reproduce the test position immediately after reaching the initial position, because the time that the limb is kept in a static position prior to the movement onset changes the accuracy of joint-position sense [28]. Joint position sense was randomly evaluated at an intermediate range of knee flexion (using a goniometer to indicate that the target angle was effectively between 40° and 60°) in which muscle mechanoreceptor input is the primary contributor to joint position sense [29]. Knee angles were determined by computer analysis of the videotaped images of the knee joint using the two-dimensional automatic digitizing module of the Ariel Performance Analysis System software (Ariel Dynamics, CA, USA) [26]. The test and the three response positions were determined as the average of seven consecutive frames digitized at 50 Hz from the videotape view of each position. Knee JPS is reported as: (i) the absolute angular error, defined as the absolute difference between the test position and the position reproduced by the subject, which represents accuracy without directional bias; the (ii) relative angular error, the signed arithmetic difference between a test and a response position, which represents accuracy with directional bias; and (iii) the variable angular error (commonly represented by the standard deviation from the mean of a set of response errors), determined as the standard deviation from the mean of the relative errors [27]. The reliability of this method of joint position sense assessment was tested in six subjects (age: 20–26 years old) outside the sample, but subject to the criteria for inclusion/exclusion previously defined, in two sessions 4 days apart. The intraclass correlation coefficient (ICC) for absolute, relative and variable angular error was ICC = 0.910, ICC = 0.809 and ICC = 0.855, respectively. For each error, the corresponding ICC was used to calculate the standard error of measurement (SEM) and, then, the SEM was used to compute the smallest real difference (SRD) [30]. The SEM for absolute, relative and variable angular errors was respectively 0.42°, 0.59, and 0.76°. The SRD for absolute, relative and variable angular errors was respectively 1.16°, 1.64°, and 2.10°. 2.4. Warm-up and football match The standardized warm-up had a duration of 25 min and comprised routine exercises for general activation and football-specific exercises. Briefly, the warm-up was performed in an official football field and was composed of jogging, skipping, dynamic mobility exercises for upper and lower body, stretching, and specific football drills (pass, ball control, and kicking). The official football match had a duration of 90 min (plus, in average, 4 min of extra time to compensate for stoppages), divided into two parts of 45 min with a 15-minute interval in between. 2.5. Statistical analyses A statistical analysis was performed using SPSS version 17.0 (SPSS Inc., Chicago, IL). The normality of data distribution was tested with
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the Shapiro–Wilk Test. Descriptive statistics were calculated. A repeated measure analysis of variance (General Linear Model) was used to test mean differences in RPE and joint-position sense between the results obtained at rest, after warming and at the end the match. Post-hoc means that comparisons were performed using Bonferroni Tests. Effect size was reported using partial eta-squared (η2p). The level of significance was set a priori as alpha = 0.05. 3. Results All 14 participants, with a mean of 16 ± 5.2 years of football experience, completed the football match and have accomplished all the procedures of the study set-up. Perceived exertion changed significantly over time (F2,26 = 125.99, p b 0.001; η2p = 0.906), it increased significantly from rest to the end of warm-up (rest: 8.6 ± 2.1, minimum: 6, maximum: 12, to after warm-up: 12.1 ± 2.0; minimum: 9, maximum 15; mean difference: − 3.5, 95% CI [− 5.1, − 1.9], p b 0.001) and to the end of the match (rest: 8.6 ± 2.1, minimum: 6, maximum: 12, to after football match: 18.5 ± 1.3, minimum 16, maximum: 20; mean difference: −9.9, 95% CI [−11.9, −7.8], p b 0.001). Perceived exertion also increased from after the pre-participation football match warm-up to the end of the match (mean difference: −6.4, 95% CI [−7.8, −4.9], p b 0.001). Absolute (F2,26 = 27.53, p b 0.001; η2p = 0.679), and relative (F2,26 = 22.90, p b 0.001; η2p = 0.638) angular errors changed significantly over time (Figs. 2 and 3, respectively). Compared to rest, after the warm-up, a significant decrease in absolute angular error was observed (4.1° ± 2.2° vs 2.0° ± 1.0°; mean difference: 2.1, 95% CI [0.4, 4.1], p = 0.045). However, after the match, absolute angular error (8.7° ± 3.8°) increased significantly comparatively to both rest (mean difference: − 4.6, 95% CI [− 7.3, − 1.9], p = 0.001) and the end of warm-up (mean difference: −6.7, 95% CI [−9.5, −3.9], p b 0.001). The relative error (Fig. 3) showed directional bias of repositioning with an underestimation of the target position at rest (−1.5° ± 4.2°), after the warm-up (−0.48° ± 2.1°), and after the match (−8.5° ± 4.1°). From the start position of 90° of flexion and using the desired movement to extend the knee, the participants did not extend the knee far enough to reach the test position determined by the examiner. This was attenuated after the warm-up (mean difference to rest: −1.1, 95% CI [−4.7, 2.6], p = 1.000), whereas match-induced fatigue significantly exacerbated the underestimation of the test position when compared to rest (mean difference: 7.0, 95% CI [3.0, 10.9], p = 0.001) and after warm-up (mean difference: 8.0, 95% CI [5.1, 10.9], p b 0.001). The variable error did not change significantly (F2,26 = 2.64, p N 0.05; η2p = 0.169) from rest (1.84° ± 0.92°) to both after the warm-up (1.28° ± 0.68°) and the end of the match (2.18° ± 1.52°).
4. Discussion The main findings of the present study indicated that knee-jointposition sense was enhanced by warm-up exercise, although it was decreased as a consequence of fatigue induced by prolonged intermittent exercise in the football match. The effect of moderate and fatiguing exercise on proprioception has been investigated using different exercise protocols [10–13,17], which limits the comparison among them. The exercise protocols used in previous research have typically failed to replicate the physical demands of a football match. One major difference of this study to others is that the induction of fatigue was not performed by scrimmages or laboratory protocols but by the subjects' participation in an actual competitive football match. In this sense, the results of the present investigation can advantageously be transferred to the athletic setting. At the end of warm-up, perceived exertion averaged 12 points (between light to somewhat hard), and at the end of the match, it averaged 18.5 points (between very hard and very, very hard), meaning that exercise intensity was adjusted to fulfill the goals of warm-up and to induce fatigue [25]. These values of rate of perceived exertion are not surprising, since it was already described that football players experience reduced performance in the later stages of the match [31]. Our results after the warm-up are similar to those reported in previous studies [10–13] and seem to support the importance of warm-up exercise. Bartlett and Warren [12] evaluated the effects of a standardized 4-minutes warm-up consisting of jogging and stretching exercises on the knee-position sense of rugby players and concluded that after a period of stretching and gentle exercise, knee proprioception is improved. A potential confounder for joint position sense accuracy measured immediately after warm-up can be the effect of previous stretching exercises performed during the warm-up. In a study aiming
Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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Fig. 2. Position matching errors (absolute error) at rest, after warm-up and at the end of the match (A) and individual responses across conditions (B).
to investigate if a stretch regimen consisting of three 30 s stretches alters the knee joint position sense [32], the authors found that the ability to reproduce the position of 45° of knee flexion is improved subsequent to a static stretch regimen, despite the lack of improvements for replicating the target position at 20° of knee flexion. However, other studies [33,34] showed that a static stretch had no effect on subsequent joint position sense measures. On the other hand all the studies above mentioned were conducted in healthy subjects and not in football players. Therefore, future studies are needed to ascertain the true effect of stretching performed during football warm-up on subsequent measures of joint position sense. Warm-up may enhance the function of muscular mechanoreceptors by improving the viscoelastic properties of muscular tissue, enhancing oxygenation, increasing the nerve-conduction rate, and increasing body temperature due to vasodilatation [8]. We are also impelled to consider a possible role of the Central Nervous System in the better position-sense accuracy observed after the warm-up. In fact, the period of warm-up could have increased muscle spindle sensitivity by changing fusimotor commands [10] and consequently decreasing knee errors in sports matches. By way of contrast to the exercise performed in the warm-up period, the subsequent football match induced a significant increase in kneejoint-position errors. Studies on muscle fatigue and its effects on proprioception grew in numbers in the past decade. The effects of exerciseinduced muscle fatigue on joint proprioception have been extensively investigated in young [21] and old-age subjects [26], in male [35] and
Fig. 3. Repositioning directional bias (relative error) at rest, after warm-up and at the end of the match. The negative values mean the underestimation of the repositioning relatively to the target position.
female subjects [18], in athletes [23,36] and non-athletes, and in several joints including the shoulder [37,38], elbow [20,39], knee [40,41], and ankle [42]. Our results are similar to those reported in studies using laboratory protocols [26,40,41], laboratory protocols replicating sporting activities [23,36], and field protocols [18], which also reported a decrease in joint-position sense after fatiguing exercise. The decrease in proprioception has been imputed to the increased concentrations of metabolites and inflammatory substances (such as lactic acid, bradykinin, serotonin, potassium, arachidonic acid and prostaglandins) within the fatigued muscle, which in turn have a direct impact on the discharge pattern of muscle spindles and alpha–gamma co-activation [43–45]. The negative effect of the football match on joint-position-sense accuracy can also be partly explained by changes in the processing of proprioceptive inputs at the central level, thereby reducing proprioceptive acuity and joint stability in response to external forces [46]. Central fatigue might have decreased the accuracy of motor control and dynamic muscle stabilization and movement efficiency during play, hence placing the knee at higher injury risk [46]. Indeed, Allen et al. [19] affirmed that despite the peripheral origin of the factors that trigger the effects of exercise on position sense, they exert their influence on proprioception centrally. We cannot say which of the mechanisms of muscle fatigue may have had a greater contribution on the modification of the accuracy and consistency of joint-position sense. In fact, to distinguish with certainty the degradation of input from among mechanoreceptors, motor control performance, and central motor programming is difficult, since any test covers all avenues of information. Regarding the directional bias in the errors, data from the present study followed the same direction as those reported previously [19, 41]. After the football match, the errors in the direction of flexion were exacerbated. Allen et al. [19] showed that exercising antagonists (knee flexors) produced errors in the same direction. Givoni et al. [41] had shown that the exercise of agonists (knee extensors) also induced errors in the direction of knee flexion. Our study involved exercising both muscle groups, knee flexors and extensors; hence, perhaps the direction of the error could be independent of the exercised muscle group. The variable error was similar in all assessments, which indicates that reduced variability in the subjects' responses was independent of exposure conditions. Some study limitations should be recognized. First, there was a lack of assessment of maximum voluntary muscle strength, which could have enabled us to provide a direct measure of muscle function to determine the changes related to exercise-induced fatigue. Second, there was no separate or randomized control group. Hence, we cannot completely exclude the possibility of learning and time effects in the results. Nevertheless, considering that the repeated assessment could have led to a learning effect, to overcome this limitation, the target angles were determined randomly between 40°–60° of knee flexion.
Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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Third, the target knee angles were defined passively (while repositioning was active), which was previously showed to be less accurate than the active positioning for the calibration of position sense [47]. Indeed, the peripheral receptors providing information to the central nervous system in active and passive modes are differently involved and thus affecting the kinesthetic sensibility [10]. However, Lloyd and Caldwell [48] found that the differences in modes for leg displacement only appeared within the customary limits of excursion of the joint, which is not the case in the present study. Fourth, because the participants were not assessed in the same match, we cannot avoid the variation of the opposition level and environmental conditions. However, environmental conditions did not differ too much from match to match, since they were played in a seasonal period where the temperatures did not vary within a high range. Furthermore, evaluations were not made on rainy days. Some questions remain to be answered in future studies, namely for how long the beneficial effect of warm-up and the deleterious effect of match-induced fatigue on joint-position sense might last. Moreover, as previous studies indicated that during match play, fatigue or reduced performance seems to occur at the end of the first half as well [31], it would be interesting to evaluate the changes in proprioception at this period. Additionally, in future studies, the inclusion of a control group is strongly recommended to account for potential learning effects. Furthermore, we cannot be certain to whether the results of the present study apply to pro/elite football players or to female footballers as well, and therefore, future studies should be conducted to answer to these questions. These are issues of undoubted importance to athletes, physiotherapists, and athletic trainers and have practical and clinical implications. First, they reinforce the value of warm-up as a tool to improve the state of readiness of football players for the match, and therefore the need to include in warm-up exercises targeting the kinesthetic senses. Secondly, since prolonged exercise have a deleterious effect on joint position sense, training schedules should be targeted to ameliorate local endurance for the improvement of the players preparedness, and to minimize exercise-induced neuromuscular fatigue. In conclusion, proprioceptive acuity is increased after warm-up exercise and decreased by football-match-induced fatigue. Despite assessing joint-position sense in an open kinetic chain, our results seem to indicate that the enhanced sensitivity of mechanoreceptors with warm-up exercises could contribute to injury prevention and improved performance during a football match, whereas the deleterious effect of match-induced fatigue on the sensorimotor system could contribute to joint instability and, ultimately, injury. Conflict of interest statement All authors declare that they do not have any conflict of interest relating to this paper. Acknowledgments The Research Centre in Physical Activity, Health and Leisure (CIAFEL) is funded by the Portuguese Foundation of Science and Technology (FTC), grant Pest-OE/SAU/UI0617/2011. We greatly appreciate the cooperation of all football players who agreed to voluntarily participate in this study. References [1] Hiemstra LA, Lo IK, Fowler PJ. Effect of fatigue on knee proprioception: implications for dynamic stabilization. J Orthop Sports Phys Ther 2001;31:598–605. [2] Ribeiro F, Oliveira J. Aging effects on joint proprioception: the role of physical activity in proprioception preservation. Eur Rev Aging Phys Act 2007;4:71–6. [3] Thacker SB, Stroup DF, Branche CM, Gilchrist J, Goodman RA, Porter Kelling E. Prevention of knee injuries in sports. A systematic review of the literature. J Sports Med Phys Fitness 2003;43:165–79.
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Contents lists available at ScienceDirect
The Knee
Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue Eduardo Salgado a, Fernando Ribeiro b, José Oliveira a,⁎ a b
University of Porto, Faculty of Sport, Research Centre in Physical Activity, Health and Leisure (CIAFEL), Porto, Portugal School of Health Sciences, University of Aveiro, Aveiro, Portugal
a r t i c l e
i n f o
Article history: Received 3 February 2014 Received in revised form 7 July 2014 Accepted 13 October 2014 Available online xxxx Keywords: Football Proprioception Warm-up Fatigue
a b s t r a c t Background: The demands to which football players are exposed during the match may augment the risk of injury by decreasing the sense of joint position. This study aimed to assess the effect of pre-participation warm-up and fatigue induced by an official football match on the knee-joint-position sense of football players. Methods: Fourteen semi-professional male football players (mean age: 25.9 ± 4.6 years old) volunteered in this study. The main outcome measures were rate of perceived exertion and knee-joint-position sense assessed at rest, immediately after a standard warm-up (duration 25 min), and immediately after a competitive football match (90 minutes duration). Results: Perceived exertion increased significantly from rest to the other assessments (rest: 8.6 ± 2.0; after warm-up: 12.1 ± 2.1; after football match: 18.5 ± 1.3; p b 0.001). Compared to rest, absolute angular error decreased significantly after the warm-up (4.1° ± 2.2° vs. 2.0° ± 1.0°; p = 0.0045). After the match, absolute angular error (8.7° ± 3.8°) increased significantly comparatively to both rest (p = 0.001) and the end of warm-up (p b 0.001). Relative error showed directional bias with an underestimation of the target position, which was higher after the football match compared to both rest (p b 0.001) and after warm-up (p b 0.001). Conclusions: The results indicate that knee-joint-position sense acuity was increased by pre-participation warm-up exercise and was decreased by football match-induced fatigue. Clinical relevance: Warm-up exercises could contribute to knee injury prevention, whereas the deleterious effect of match-induced fatigue on the sensorimotor system could ultimately contribute to knee instability and injury. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Proprioception contributes to several conscious and unconscious sensations, automatic control of movement, balance and postural control, and joint stability, as a result of neural cumulative input to the central nervous system proceeding from specialized nerve endings called mechanoreceptors [1,2]. Joint position sense (JPS), a sub-modality of proprioception, is generally defined as the awareness of the joint position and represents the ability to identify and reproduce a joint angle after the limb has been moved [1]. In sports activities, like football, joint position sense acuity could be paramount for overall performance, since it is related with the level of skills accuracy [2] and the risk of injury [3]. Indeed, changes in the state of the muscle induced by moderate-intensity, warm-up exercise, or muscle fatigue induced by high-intensity exercise could have repercussions on the muscular receptors, which are described as the main sources of afferent information contributing to joint-position sense [4, ⁎ Corresponding author at: Research Centre in Physical Activity, Health and Leisure (CIAFEL), Faculty of Sport, University of Porto, Rua Dr. Plácido Costa, 91, 4200-450 Porto, Portugal. Tel.: +351 22 5074773; fax: +351 22 5500689. E-mail address: [email protected] (J. Oliveira).
5]. However, the repercussions of exercise-induced fatigue on muscle receptors are controversial, as there are studies in cats showing that fatiguing eccentric muscle contractions have no repercussions on the muscle receptors [6,7]. Warm-up exercises are recognized to have positive effects on performance by reducing muscle stiffness, ameliorating the viscoelastic function of structures surrounding the joints, and increasing neural conduction and velocity, and metabolic efficiency [8,9]. However, only few studies [10–13] have been conducted evaluating the effect of warm-up on proprioception. Despite using different warm-up protocols and different methods to measure proprioception, these studies reported positive effects on knee proprioception after warm-up. On the other hand, high intensity exercise is associated with the reduction of muscle force, joint range of motion, and joint stability. It is also associated with clumsiness in movements demanding high levels of accuracy [14–17]. Several studies have shown that immediately after strenuous exercise, the size of the errors observed during positionmatching tasks increases significantly [18–20]. Investigations targeting the effects of mild intensity warm-up exercise and exercise-induced muscle fatigue on joint-position sense acuity have rarely been conducted in athletes. Additionally, the exercise protocols commonly used do not mimic the specific demands of
http://dx.doi.org/10.1016/j.knee.2014.10.002 0968-0160/© 2015 Elsevier B.V. All rights reserved.
Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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sporting activities. To our knowledge, few studies [18,21] assessed changes in proprioception induced by sporting activities. It is established that pre-participation warm-up improves physical performance [9], which could be explained, at least partially, by the improvement of sense of limb position. Conversely, the prolonged duration and intense muscle demands to which football players are exposed during the match might have deleterious effects on knee-joint-position sense, hence decreasing the sense of limb position, increasing errors, and augmenting the risk of injury [3]. Thus, the purpose of the present study was to assess the effect of pre-participation warm-up and fatigue induced by an official football match on knee-joint-position sense in football players. We hypothesize that pre-participation warm-up will improve knee position sense, whereas the football match will reduce knee position sense to values below those observed at rest. In this sense, if our hypothesis is confirmed, it will reinforce the importance of warming-up before a football match and reinforce the need to improve strategies to attenuate the impact of fatigue on joint proprioception in order to decrease the risk of injuries. 2. Methods 2.1. Participants and study design Fourteen healthy adult male semi-professional football players volunteered to participate in this study (mean age: 25.9 ± 4.6 years old, mean height: 179 ± 5 cm, mean weight: 75.4 ± 3.5 kg). The statistical power for the matched pairs analysis was computed a priori to establish the necessary sample size to achieve 95% power with α = 5% to detect differences in absolute angular error between the baseline and post-warm-up or post-match. This calculation was performed based on data presented in previous studies, respectively for baseline– warm-up [10] and baseline–end of the match [18]. It revealed that 14 participants were required (including a possible drop-out rate of three participants). Participants were volunteers recruited from a semi-professional football team. To be included in the study, participants had to have practiced football for more than 8 years (to minimize any possible influence of training and competitive experience on jointposition sense) with a frequency of at least three times per week and a normal knee range of motion. Participants were excluded according to the following criteria: lower limb or lower back injury in the 6 months before the study, history of knee surgery, taking medication with an influence on motor control and/or attention, and vestibular or neuromuscular disorders. Appropriate ethical approval from our institutional board was granted prior to the commencement of the study. All participants provided written, informed consent, and all procedures were conducted according the declaration of Helsinki. The study design is depicted in Fig. 1. In brief, the recruitment and selection of the participants was performed 1 month before starting data collection. The rate of perceived exertion (RPE) [22] and knee-joint-position sense were measured at rest, immediately after a standard warm-up (duration 25 min) and immediately after a competitive football match (approximate time slot of 90 min plus, on average, 4 min of extra time due to stoppages). Due to the time required to assess joint-position sense and in order to avoid the disappearance of the acute effects of both the warm-up and match on joint-position sense, only two players were evaluated in each game. Additionally, since the games where the data was collected were official competitive games, the time between warm-up and the start of the game was very small, thus leaving little room for the joint-position sense assessment. As a result, a total of seven competitive games, from February to April, were covered to collect data from 14 players. 2.2. Evaluation of rate of perceived exertion The evaluation of the rate of perceived exertion (RPE) was performed using Borg's rating-of-perceived-exertion scale (scale of 6 to
Fig. 1. Study timeline and design.
20 points) [22]. The RPE scale was used to evaluate the exercise intensity during the warm-up and the football match. Participants were considered to be fatigued if they reported an RPE of 15 or above [23,24]. Indeed, a score of 15 was reported as being strongly correlated with the metabolic responses of fatigue [25]. 2.3. Evaluation of joint-position sense Knee-joint-position sense of the dominant limb was evaluated using a technique of open-kinetic chain and active knee positioning of a passively determined position [26]. The technique was ipsilateral and performed without visual input [26]. The dominant limb was determined by asking which lower limb they normally use to shoot, pass and tackle. The dominant limb was the right lower limb in all the participants. The same examiner conducted all the procedures. Additionally, the matches were always on Sundays at 3 p.m. Prior to the joint-position-sense assessment, four reflective markers were fixed with double-sided adhesive tape to the skin of the apex of the greater trochanter; the iliotibial tract, level with the posterior crease of the knee when flexed to 80°; the head of the fibula; and the prominence of the lateral malleolus [26,27]. Since the markers were removed after each evaluation, their places were marked on the skin to avoid differences among evaluations. Each pair of markers represents the axis of the thigh and the leg. To record the joint positions, a tripodmounted video camera was used. It was positioned 7 m away from the participant – at the same level as the knee joint – and then manually focused on the field of view. The camera was in the sagittal plane. The same video camera was used over the experimental period. Natural vertical and horizontal lines in the videotaped environment were aligned parallel to the horizontal and vertical edges of the viewfinder to minimize camera tilt. To evaluate joint-position sense, participants, wearing shorts, were seated on a physiotherapy treatment table with their legs hanging freely but not touching the ground, and were blindfolded to remove visual input. To avoid verbal-sound cues, all the evaluations took place in a
Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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silent room, and only the examined athlete and the investigator were inside. The starting position was 90° of knee flexion and the repositioning movement was into knee extension. The examiner slowly (at approximately 10°/s) moved the leg from the starting position (90° of knee flexion) to a random knee angle between 40° and 60° of flexion. Then, the subject maintained the test position actively for 5 s in order to identify (memorize) that position. After that, the subject was instructed by the examiner to actively return the leg to the starting position and to immediately extend the knee actively in an attempt (upon the command “reposition”) to reproduce the test position using the same limb. The subject then returned to the position perceived as the test position and reported “target” to the examiner. This position was held for 5 s, and on the command “return,” the subject returned to the initial position and repeated the repositioning twice. Thus, subjects performed three repetitions (actively reproduced knee angle) in order to reproduce one target angle (passively positioned knee angle). The participants were told to reproduce the test position immediately after reaching the initial position, because the time that the limb is kept in a static position prior to the movement onset changes the accuracy of joint-position sense [28]. Joint position sense was randomly evaluated at an intermediate range of knee flexion (using a goniometer to indicate that the target angle was effectively between 40° and 60°) in which muscle mechanoreceptor input is the primary contributor to joint position sense [29]. Knee angles were determined by computer analysis of the videotaped images of the knee joint using the two-dimensional automatic digitizing module of the Ariel Performance Analysis System software (Ariel Dynamics, CA, USA) [26]. The test and the three response positions were determined as the average of seven consecutive frames digitized at 50 Hz from the videotape view of each position. Knee JPS is reported as: (i) the absolute angular error, defined as the absolute difference between the test position and the position reproduced by the subject, which represents accuracy without directional bias; the (ii) relative angular error, the signed arithmetic difference between a test and a response position, which represents accuracy with directional bias; and (iii) the variable angular error (commonly represented by the standard deviation from the mean of a set of response errors), determined as the standard deviation from the mean of the relative errors [27]. The reliability of this method of joint position sense assessment was tested in six subjects (age: 20–26 years old) outside the sample, but subject to the criteria for inclusion/exclusion previously defined, in two sessions 4 days apart. The intraclass correlation coefficient (ICC) for absolute, relative and variable angular error was ICC = 0.910, ICC = 0.809 and ICC = 0.855, respectively. For each error, the corresponding ICC was used to calculate the standard error of measurement (SEM) and, then, the SEM was used to compute the smallest real difference (SRD) [30]. The SEM for absolute, relative and variable angular errors was respectively 0.42°, 0.59, and 0.76°. The SRD for absolute, relative and variable angular errors was respectively 1.16°, 1.64°, and 2.10°. 2.4. Warm-up and football match The standardized warm-up had a duration of 25 min and comprised routine exercises for general activation and football-specific exercises. Briefly, the warm-up was performed in an official football field and was composed of jogging, skipping, dynamic mobility exercises for upper and lower body, stretching, and specific football drills (pass, ball control, and kicking). The official football match had a duration of 90 min (plus, in average, 4 min of extra time to compensate for stoppages), divided into two parts of 45 min with a 15-minute interval in between. 2.5. Statistical analyses A statistical analysis was performed using SPSS version 17.0 (SPSS Inc., Chicago, IL). The normality of data distribution was tested with
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the Shapiro–Wilk Test. Descriptive statistics were calculated. A repeated measure analysis of variance (General Linear Model) was used to test mean differences in RPE and joint-position sense between the results obtained at rest, after warming and at the end the match. Post-hoc means that comparisons were performed using Bonferroni Tests. Effect size was reported using partial eta-squared (η2p). The level of significance was set a priori as alpha = 0.05. 3. Results All 14 participants, with a mean of 16 ± 5.2 years of football experience, completed the football match and have accomplished all the procedures of the study set-up. Perceived exertion changed significantly over time (F2,26 = 125.99, p b 0.001; η2p = 0.906), it increased significantly from rest to the end of warm-up (rest: 8.6 ± 2.1, minimum: 6, maximum: 12, to after warm-up: 12.1 ± 2.0; minimum: 9, maximum 15; mean difference: − 3.5, 95% CI [− 5.1, − 1.9], p b 0.001) and to the end of the match (rest: 8.6 ± 2.1, minimum: 6, maximum: 12, to after football match: 18.5 ± 1.3, minimum 16, maximum: 20; mean difference: −9.9, 95% CI [−11.9, −7.8], p b 0.001). Perceived exertion also increased from after the pre-participation football match warm-up to the end of the match (mean difference: −6.4, 95% CI [−7.8, −4.9], p b 0.001). Absolute (F2,26 = 27.53, p b 0.001; η2p = 0.679), and relative (F2,26 = 22.90, p b 0.001; η2p = 0.638) angular errors changed significantly over time (Figs. 2 and 3, respectively). Compared to rest, after the warm-up, a significant decrease in absolute angular error was observed (4.1° ± 2.2° vs 2.0° ± 1.0°; mean difference: 2.1, 95% CI [0.4, 4.1], p = 0.045). However, after the match, absolute angular error (8.7° ± 3.8°) increased significantly comparatively to both rest (mean difference: − 4.6, 95% CI [− 7.3, − 1.9], p = 0.001) and the end of warm-up (mean difference: −6.7, 95% CI [−9.5, −3.9], p b 0.001). The relative error (Fig. 3) showed directional bias of repositioning with an underestimation of the target position at rest (−1.5° ± 4.2°), after the warm-up (−0.48° ± 2.1°), and after the match (−8.5° ± 4.1°). From the start position of 90° of flexion and using the desired movement to extend the knee, the participants did not extend the knee far enough to reach the test position determined by the examiner. This was attenuated after the warm-up (mean difference to rest: −1.1, 95% CI [−4.7, 2.6], p = 1.000), whereas match-induced fatigue significantly exacerbated the underestimation of the test position when compared to rest (mean difference: 7.0, 95% CI [3.0, 10.9], p = 0.001) and after warm-up (mean difference: 8.0, 95% CI [5.1, 10.9], p b 0.001). The variable error did not change significantly (F2,26 = 2.64, p N 0.05; η2p = 0.169) from rest (1.84° ± 0.92°) to both after the warm-up (1.28° ± 0.68°) and the end of the match (2.18° ± 1.52°).
4. Discussion The main findings of the present study indicated that knee-jointposition sense was enhanced by warm-up exercise, although it was decreased as a consequence of fatigue induced by prolonged intermittent exercise in the football match. The effect of moderate and fatiguing exercise on proprioception has been investigated using different exercise protocols [10–13,17], which limits the comparison among them. The exercise protocols used in previous research have typically failed to replicate the physical demands of a football match. One major difference of this study to others is that the induction of fatigue was not performed by scrimmages or laboratory protocols but by the subjects' participation in an actual competitive football match. In this sense, the results of the present investigation can advantageously be transferred to the athletic setting. At the end of warm-up, perceived exertion averaged 12 points (between light to somewhat hard), and at the end of the match, it averaged 18.5 points (between very hard and very, very hard), meaning that exercise intensity was adjusted to fulfill the goals of warm-up and to induce fatigue [25]. These values of rate of perceived exertion are not surprising, since it was already described that football players experience reduced performance in the later stages of the match [31]. Our results after the warm-up are similar to those reported in previous studies [10–13] and seem to support the importance of warm-up exercise. Bartlett and Warren [12] evaluated the effects of a standardized 4-minutes warm-up consisting of jogging and stretching exercises on the knee-position sense of rugby players and concluded that after a period of stretching and gentle exercise, knee proprioception is improved. A potential confounder for joint position sense accuracy measured immediately after warm-up can be the effect of previous stretching exercises performed during the warm-up. In a study aiming
Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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Fig. 2. Position matching errors (absolute error) at rest, after warm-up and at the end of the match (A) and individual responses across conditions (B).
to investigate if a stretch regimen consisting of three 30 s stretches alters the knee joint position sense [32], the authors found that the ability to reproduce the position of 45° of knee flexion is improved subsequent to a static stretch regimen, despite the lack of improvements for replicating the target position at 20° of knee flexion. However, other studies [33,34] showed that a static stretch had no effect on subsequent joint position sense measures. On the other hand all the studies above mentioned were conducted in healthy subjects and not in football players. Therefore, future studies are needed to ascertain the true effect of stretching performed during football warm-up on subsequent measures of joint position sense. Warm-up may enhance the function of muscular mechanoreceptors by improving the viscoelastic properties of muscular tissue, enhancing oxygenation, increasing the nerve-conduction rate, and increasing body temperature due to vasodilatation [8]. We are also impelled to consider a possible role of the Central Nervous System in the better position-sense accuracy observed after the warm-up. In fact, the period of warm-up could have increased muscle spindle sensitivity by changing fusimotor commands [10] and consequently decreasing knee errors in sports matches. By way of contrast to the exercise performed in the warm-up period, the subsequent football match induced a significant increase in kneejoint-position errors. Studies on muscle fatigue and its effects on proprioception grew in numbers in the past decade. The effects of exerciseinduced muscle fatigue on joint proprioception have been extensively investigated in young [21] and old-age subjects [26], in male [35] and
Fig. 3. Repositioning directional bias (relative error) at rest, after warm-up and at the end of the match. The negative values mean the underestimation of the repositioning relatively to the target position.
female subjects [18], in athletes [23,36] and non-athletes, and in several joints including the shoulder [37,38], elbow [20,39], knee [40,41], and ankle [42]. Our results are similar to those reported in studies using laboratory protocols [26,40,41], laboratory protocols replicating sporting activities [23,36], and field protocols [18], which also reported a decrease in joint-position sense after fatiguing exercise. The decrease in proprioception has been imputed to the increased concentrations of metabolites and inflammatory substances (such as lactic acid, bradykinin, serotonin, potassium, arachidonic acid and prostaglandins) within the fatigued muscle, which in turn have a direct impact on the discharge pattern of muscle spindles and alpha–gamma co-activation [43–45]. The negative effect of the football match on joint-position-sense accuracy can also be partly explained by changes in the processing of proprioceptive inputs at the central level, thereby reducing proprioceptive acuity and joint stability in response to external forces [46]. Central fatigue might have decreased the accuracy of motor control and dynamic muscle stabilization and movement efficiency during play, hence placing the knee at higher injury risk [46]. Indeed, Allen et al. [19] affirmed that despite the peripheral origin of the factors that trigger the effects of exercise on position sense, they exert their influence on proprioception centrally. We cannot say which of the mechanisms of muscle fatigue may have had a greater contribution on the modification of the accuracy and consistency of joint-position sense. In fact, to distinguish with certainty the degradation of input from among mechanoreceptors, motor control performance, and central motor programming is difficult, since any test covers all avenues of information. Regarding the directional bias in the errors, data from the present study followed the same direction as those reported previously [19, 41]. After the football match, the errors in the direction of flexion were exacerbated. Allen et al. [19] showed that exercising antagonists (knee flexors) produced errors in the same direction. Givoni et al. [41] had shown that the exercise of agonists (knee extensors) also induced errors in the direction of knee flexion. Our study involved exercising both muscle groups, knee flexors and extensors; hence, perhaps the direction of the error could be independent of the exercised muscle group. The variable error was similar in all assessments, which indicates that reduced variability in the subjects' responses was independent of exposure conditions. Some study limitations should be recognized. First, there was a lack of assessment of maximum voluntary muscle strength, which could have enabled us to provide a direct measure of muscle function to determine the changes related to exercise-induced fatigue. Second, there was no separate or randomized control group. Hence, we cannot completely exclude the possibility of learning and time effects in the results. Nevertheless, considering that the repeated assessment could have led to a learning effect, to overcome this limitation, the target angles were determined randomly between 40°–60° of knee flexion.
Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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Third, the target knee angles were defined passively (while repositioning was active), which was previously showed to be less accurate than the active positioning for the calibration of position sense [47]. Indeed, the peripheral receptors providing information to the central nervous system in active and passive modes are differently involved and thus affecting the kinesthetic sensibility [10]. However, Lloyd and Caldwell [48] found that the differences in modes for leg displacement only appeared within the customary limits of excursion of the joint, which is not the case in the present study. Fourth, because the participants were not assessed in the same match, we cannot avoid the variation of the opposition level and environmental conditions. However, environmental conditions did not differ too much from match to match, since they were played in a seasonal period where the temperatures did not vary within a high range. Furthermore, evaluations were not made on rainy days. Some questions remain to be answered in future studies, namely for how long the beneficial effect of warm-up and the deleterious effect of match-induced fatigue on joint-position sense might last. Moreover, as previous studies indicated that during match play, fatigue or reduced performance seems to occur at the end of the first half as well [31], it would be interesting to evaluate the changes in proprioception at this period. Additionally, in future studies, the inclusion of a control group is strongly recommended to account for potential learning effects. Furthermore, we cannot be certain to whether the results of the present study apply to pro/elite football players or to female footballers as well, and therefore, future studies should be conducted to answer to these questions. These are issues of undoubted importance to athletes, physiotherapists, and athletic trainers and have practical and clinical implications. First, they reinforce the value of warm-up as a tool to improve the state of readiness of football players for the match, and therefore the need to include in warm-up exercises targeting the kinesthetic senses. Secondly, since prolonged exercise have a deleterious effect on joint position sense, training schedules should be targeted to ameliorate local endurance for the improvement of the players preparedness, and to minimize exercise-induced neuromuscular fatigue. In conclusion, proprioceptive acuity is increased after warm-up exercise and decreased by football-match-induced fatigue. Despite assessing joint-position sense in an open kinetic chain, our results seem to indicate that the enhanced sensitivity of mechanoreceptors with warm-up exercises could contribute to injury prevention and improved performance during a football match, whereas the deleterious effect of match-induced fatigue on the sensorimotor system could contribute to joint instability and, ultimately, injury. Conflict of interest statement All authors declare that they do not have any conflict of interest relating to this paper. Acknowledgments The Research Centre in Physical Activity, Health and Leisure (CIAFEL) is funded by the Portuguese Foundation of Science and Technology (FTC), grant Pest-OE/SAU/UI0617/2011. We greatly appreciate the cooperation of all football players who agreed to voluntarily participate in this study. References [1] Hiemstra LA, Lo IK, Fowler PJ. Effect of fatigue on knee proprioception: implications for dynamic stabilization. J Orthop Sports Phys Ther 2001;31:598–605. [2] Ribeiro F, Oliveira J. Aging effects on joint proprioception: the role of physical activity in proprioception preservation. Eur Rev Aging Phys Act 2007;4:71–6. [3] Thacker SB, Stroup DF, Branche CM, Gilchrist J, Goodman RA, Porter Kelling E. Prevention of knee injuries in sports. A systematic review of the literature. J Sports Med Phys Fitness 2003;43:165–79.
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Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002
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Please cite this article as: Salgado E, et al, Joint-position sense is altered by football pre-participation warm-up exercise and match induced fatigue, Knee (2015), http://dx.doi.org/10.1016/j.knee.2014.10.002