Neuroscience Letters 556 (2013) 118–123

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Attentional demands of postural control during single leg stance in patients with anterior cruciate ligament reconstruction Hossein Negahban, Payam Ahmadi, Reza Salehi ∗ , Mohammad Mehravar, Shahin Goharpey Musculoskeletal Rehabilitation Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

h i g h l i g h t s • Poor postural stability was seen in ACL-R patients compared to healthy controls. • ACL-R patients showed poor postural stability in dual-compared to single-task. • Posture-cognition interference was not observed in healthy control participants.

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Article history: Received 7 July 2013 Received in revised form 9 October 2013 Accepted 11 October 2013 Keywords: Attention Cognition Posture Anterior cruciate ligament Reconstruction

a b s t r a c t The aim of this study was to investigate the amount of attention demands of postural control in patients with anterior cruciate ligament-reconstruction (ACL-R), by comparing the pattern of posture-cognition interaction between two groups of ACL-R patients (n = 25) and healthy matched controls (n = 25). All participants were examined during single-leg stance on a balance board under both single- and dualtask conditions in 4 dynamic balance tests. These tests were standing on the injured and uninjured legs with straight or flexed knees. The corresponding dominant and non-dominant legs of healthy group were considered as controls. Contact frequency and contact time were acquired as a measure of postural performance. Cognitive performance was assessed by counting the number of errors in a silent backward digit span task. The results of analysis of variance showed a significant higher contact frequency and longer contact time in patients with ACL-R compared to healthy matched controls (p < 0.02). Moreover, the ACL-R patients showed a significantly higher contact frequency and longer contact time during dualtask compared to single-task conditions (p < 0.01). This pattern of posture-cognition interference was not observed in the healthy control group. In conclusion, patients who had undergone ACL-R surgery demonstrated poorer balance stability during single-leg stance than healthy controls. Also, simultaneous execution of the cognitive task during standing caused a significant deterioration in postural stability which indicates decreased automaticity (increased attention demanding) of postural control in patients with ACL-R compared to healthy controls. © 2013 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Anterior cruciate ligament (ACL) injury that accounts for 50% of all knee ligamentous injuries [1] commonly occurs in recreational and competitive sports activities [4]. ACL-reconstruction (ACL-R) surgery is usually recommended for those individuals who wish to return to full functional activities including sports participation [7,9,10]. Regaining neuromuscular control especially optimal postural control, after ACL-R surgery, is an important prerequisite for a safe return to sports activities [5].

∗ Corresponding author. Tel.: +98 611 374 3101. E-mail address: [email protected] (R. Salehi). 0304-3940/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2013.10.022

Howells et al. [7], in a recent systematic review, reported a trend toward impaired postural control during quiet standing in patients with ACL-R compared to healthy controls. As this impairment was more apparent and also more consistent in dynamic balance conditions (relative to static ones), they recommended evaluation of postural performance under dynamic conditions of standing balance for future studies [7]. A decrease in either of the sensory (i.e. proprioceptive deficit) or motor (i.e. muscle weakness) system functions has been proposed to be associated with impaired postural control in patients with ACL-R. However, the role of cognitive (attentional) process as a third component of postural control system remained unclear in this patient population. To investigate the role of attentional process invested in postural control, a dual-task paradigm in which a postural task was performed simultaneously with an attention challenging cognitive

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task was used [2,19]. According to limited capacity theory of attention, if simultaneous execution of standing balance control and cognitive task occupies attention more than the existing capacity, performance deterioration of one or both tasks would occur. Such performance deterioration is known as posture-cognition interference [19]. Based on this rationale, some studies have investigated the effects of performing a secondary cognitive task on postural control of patients with different musculoskeletal disorders such as ACL injury [11], low back pain (LBP) [15] and functional ankle instability (FAI) [14]. Posture-cognition interference was only reported in the FAI in which standing balance control was evaluated on dynamic platform of the Biodex Balance System (BBS) [14]. No interference was seen for the ACL-injured and LBP patients in whom postural control was assessed during standing on static platform of a fixed force plate [11,15]. Those researchers recommended using more challenging dynamic balance conditions for future investigation on posture-cognition interaction. In the current study, it was hypothesized that the pattern of posture-cognition interaction in dynamic balance conditions may be different in patients with ACL-R compared to healthy individuals. However, to our knowledge, no study has yet investigated this interaction. Therefore, the aim of this study was to investigate the amount of attentional demands of postural control in patients with ACL-R by comparing the pattern of posture-cognition interaction between two groups of patients and healthy matched controls while participants were standing on a dynamic platform of a balance board.

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Fig. 1. A schematic picture of the IWB.

Tegner activity rating scale, respectively. The KOOS has five subscales (i.e. pain, symptom, activities of daily living, sport/recreation, and quality of life) with a scoring range of 0–100 in which higher scores represent better knee function [16]. All patients had a full score of 100 for all but symptom and quality of life subscales with 98.8 ± 1.8 and 95.2 ± 5.1 points, respectively. The Tegner scale has a scoring range of 0–10 in which higher score represents higher level of physical activity [12]. The Persian-version of these instruments has acceptable psychometric properties for patients with different knee injuries including ACL injury [12,16]. 2.2. Postural task

2. Materials and methods 2.1. Participants All participants read and completed an informed consent form, and the study was approved by the local Ethics Committee. Twentyfive male patients were recruited. Recruitment was performed by telephone contact after extracting the information provided in the medical records of the patients from two physical therapy clinics in Khuzestan. The majority of the patients had been injured during recreational football (soccer) playing. The patients had undergone complete unilateral ACL-R surgery (arthroscopy) with autogenous hamstring tendon graft. From all patients, 17 (68%) had an operation on the right knee; 8 (32%) had an operation on the left knee; 19 (76%) had undergone surgery of the dominant leg; and 6 (24%) had undergone surgery of the non-dominant leg. Patients who met the following criteria were included in the current study: (1) age between 17 and 45 years old; (2) time elapsed since surgery >1 years; (3) full active range of motion of the reconstructed knee; and (4) full return to their pre-injury activity level [20]. Patients were excluded if they had (1) injury to other knee ligaments at the time of ACL rupture [6]; (2) history of injury or surgery to the ankle and hip joints of the reconstructed side [9]; (3) history of injury or surgery to the contralateral leg [9]; (4) history of recent neck and back pain [4]; (5) history of vestibular or neurological disorders [4]; (6) uncorrected visual impairment [4]; and (7) pain and joint effusion at the time of testing [10]. The mean time since surgery and time of rehabilitation was 14.1 ± 1.7 months and 37.6 ± 12.6 days, respectively. The control group (n = 25) consisted of participants who reported no history of significant musculoskeletal conditions or balance-related disorders [5,6]. They were matched with the patients according to age (24.9 ± 3.8 vs. 24.9 ± 4.3 yr), height (175.2 ± 6.8 vs. 176.2 ± 6.6 cm), weight (75.4 ± 8.6 vs. 75.5 ± 8.8 kg), and activity level (7.4 ± 0.8 vs. 7.4 ± 0.8 point). Disability and activity levels of the participants were evaluated using knee injury osteoarthritis outcome score (KOOS) and

Postural control was evaluated during single leg stance on an instrumented wobble board (IWB) (Fig. 1). The information provided in a study by O’Connell et al. [13] was used for construction of the IWB. Similar to our study, in the O’Connell et al. study, dynamic standing balance was evaluated using the IWB for evaluation of patients with ACL injury. This instrument has a flat wooden disk with a diameter of 51 cm and height of 1 cm. The wooden disk was put on a base block. In the middle of the bottom surface of the wooden disk, there was a rounded steel block (20 cm across and 1.5 cm depth of the apex). Eight micro-switches were installed on the base block. The switches were positioned under the wooden disk, on the periphery of a co-centered circle with a 50 cm diameter, and apart from each other at equal distances. A 3.5◦ angular sway was needed for contact between the edge of the wooden disk and the micro-switches. Micro-switches were interfaced with the computer through a data acquisition card (USB-4711a, Advantech Ltd., Taiwan). A custom written program in Labview (LabVIEW 2010, National Instruments) was used to control the test parameters and calculate contact frequency and contact time. Contact frequency is the number of contacts in 30 s. Contact time is the total time (in seconds) that the wooden plate is in contact with the base block (at least one micro-switch in ON). Longer contact time indicates more difficulty recovering balance after loosing it. Postural performance was determined by the ability of the participant to keep the wobble board in center. Therefore, higher contact frequency and longer contact time indicate a greater difficulty of participants to maintain the platform in stable boundaries and may represent poor balance stability. Measurements were made at a sampling rate of 100 Hz. To evaluate the reliability of the extracted parameters used in this study, 10 of the 25 healthy participants, with a mean age, height and weight of 24.6 ± 4.06 years, 176.4 ± 8.63 cm and 77.3 ± 8.12 kg, respectively, participated in the test and retest sessions with 48 h interval. In this reliability study, the order of postural conditions was randomly assigned between the two sessions. Participants were asked to stand barefoot on one leg with arms hanging relaxed at the sides and the hip-knee of the non-weight bearing leg was in 90◦ –90◦ flexion. Postural conditions used in this

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study were as follows: (1) standing on the injured leg with straight knee; (2) standing on the injured leg with flexed knee (20◦ ); (3) standing on the uninjured leg with straight knee; (4) standing on the uninjured leg with flexed knee (20◦ ). The corresponding dominant and non-dominant legs of the control group were used to test dynamic standing balance of the healthy participants. The leg used to kick a ball from standing position was considered as the dominant leg [4]. 2.3. Cognitive task The cognitive task used in this study was a silent backward digit span task [11,14,15]. This mental rehearsal task prevents sensorymotor disturbances that may occur during some visual, verbal or manual cognitive tasks while maintaining standing balance [11]. This task requires participants to hold a string of random digits in mind while rehearsing it in reverse order. Task difficulty was manipulated by varying the length of the digit string relative to the individual’s maximum digit span. Maximum digit span was determined by administering a backward digit test of the Wechsler intelligence scale [8]. The maximum number of digits recalled plus one constituted the number of digits presented in the difficult cognitive condition. The easy cognitive condition presented half of the digits of the difficult condition, rounded up when the number was odd [11,15]. Random number sequences were generated by a computer and provided via headphones to participants. Cognitive performance was evaluated by counting the number of cognitive errors in the form of intrusions, omissions, and order errors [11,15].

2.5. Statistical analysis Data were analyzed using the Statistical Package for the Social Sciences version 16.0 (SPSS Inc., Chicago, IL, USA). The mean values of the 3 trials during each experimental condition were used for statistical analysis. To evaluate the normality of data distributions, data from the postural and cognitive measures were subjected to the Kolmogorov–Smirnov (K–S) test [3]. The results of K–S test showed that both postural stability measures were distributed normally within each group (p > 0.05). However, since the cognitive errors were not normally distributed (p < 0.05), a logarithmic transformation was applied to the data prior to performing the statistical analysis [3]. Test–retest reliability of postural stability measures extracted from the IWB was evaluated by the two-way random effects model of intraclass correlation coefficient (ICC) and 95% confidence interval (95% CI) [17]. An ICC equal to or greater than 0.70 was considered acceptable for test–retest reliability. To examine postural performance, a 2 × 4 × 3 (2 groups; 4 levels of postural conditions; 3 levels of cognitive difficulty) mixed model of analysis of variance (ANOVA) was used to determine the main effects and interactions of these factors for each of the postural stability measures [3]. With regard to examination of cognitive performance, because all cognitive errors were made in the difficult cognitive task condition a 2 × 5 (2 groups; 5 levels of postural conditions) mixed model of ANOVA was used to detect possible main effects and interactions on the transformed errors of the difficult cognitive task. Alpha was set at 0.05 for all statistical analyses.

2.4. Procedure

3. Results

Because of the interacting effects between the two postural and cognitive tasks, we should examine the “performance tradeoff” in experiments with dual-task paradigm. Therefore, two outcomes of interest that should be examined are (1) the effects of cognitive loading on postural performance and (2) the effect of postural conditions on cognitive performance [19]. The dependent variables were postural stability measures (including contact frequency and contact time) and cognitive errors for the first and second outcomes of interest, respectively. To evaluate the effects of cognitive loading on postural performance, 4 levels of postural conditions (injured leg with straight knee, injured leg with flexed knee, uninjured leg with straight knee, uninjured leg with flexed knee) and 3 levels of cognitive difficulty (no-, easy-, and difficult-cognitive tasks) were combined. Standing with no cognitive task was considered as a “control” condition for postural performance. Additionally, to investigate the effects of postural conditions on cognitive performance, 5 levels of postural conditions (sitting, injured leg with straight knee, injured leg with flexed knee, uninjured leg with straight knee, uninjured leg with flexed knee) and 2 levels of cognitive difficulty (easy- and difficult-cognitive tasks) were combined. In the sitting condition, the participants were asked to sit normally on a chair without any postural data collection. Evaluating cognitive errors in sitting position was considered as a control condition for cognitive performance. In summary, each participant was exposed to 14 experimental conditions. Prior to beginning the test trials, each participant had several familiarization trials while standing on the balance board with and without performing concurrent cognitive task. Each participant performed three 30-s trials, separated by 1-min rest, in each experimental condition. The order of experimental conditions was randomized to avoid learning and fatigue effects. Also, a rest period of 5 min was provided between each experimental condition to avoid fatigue.

3.1. Test–retest reliability The results of test–retest reliability indicated an acceptable level of ICC > 0.70 for both contact frequency and contact time in most experimental conditions. The ICC (95% CI) scores of 0.88 (0.37–0.97), 0.95 (0.75–0.99), and 0.80 (0.15–0.95) were obtained for contact frequency when participants were asked to stand on the dominant leg with straight knee in the no-, easy- and difficult-cognitive tasks, respectively. Also, the ICC (95% CI) scores of 0.74 (−0.11 to 0.93), 0.79 (0.23–0.94), and 0.78 (0.07–0.94) were obtained for contact frequency when participants stood on the dominant leg with flexed knee in the no-, easy- and difficultcognitive tasks, respectively. Moreover, the ICC (95% CI) scores of 0.85 (0.38–0.96), 0.68 (−0.21 to 0.92), and 0.72 (−0.17 to 0.93) were obtained for contact time when participants were asked to stand on the dominant leg with straight knee in the no-, easy- and difficultcognitive tasks, respectively. Finally, the ICC (95% CI) scores of 0.84 (0.36–0.96), 0.70 (−0.02 to 0.92), and 0.55 (−1.02 to 0.89) were obtained for contact time when participants stood on the dominant leg with flexed knee in the no-, easy- and difficult-cognitive tasks, respectively. 3.2. Postural performance Fig. 2 shows the mean and standard error of the mean (SEM) of postural stability measures in different experimental conditions. There was no significant interaction of group by postural conditions by cognitive difficulty levels for any of the postural stability measures (F6, 288 = 0.97, P = 0.44 and F6, 288 = 1.29, P = 0.27 for contact frequency and contact time, respectively). However, the interaction of group by cognitive difficulty was significant for both postural stability measures (F2, 96 = 5.10, P < 0.01 and F2, 96 = 3.27, P = 0.04 for contact frequency and contact time, respectively). For the contact frequency, the results of the repeated measures ANOVA

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Experimental condions Fig. 2. The mean and standard error of the mean (SEM) for postural stability measures (contact frequency (A) and contact time (B)) in different experimental conditions for both study groups. ISN: injured limb, straight knee – no cognitive task; ISE: injured limb, straight knee – easy cognitive task; ISD: injured limb, straight knee – difficult cognitive task. IFN: injured limb, flexed knee – no cognitive task; IFE: injured limb, flexed knee – easy cognitive task; IFD: injured limb, flexedknee – difficult cognitive task. USN: uninjured limb, straight knee – no cognitive task; USE: uninjured limb, straight knee – easy cognitive task; USD: uninjured limb, straight knee – difficult cognitive task. UFN: uninjured limb, flexed knee – no cognitive task; UFE: uninjured limb, flexed knee – easy cognitive task; UFD: uninjured limb, flexed knee – difficult cognitive task.

showed a significant effect of cognitive loading on postural stability measures of the patients (F2, 198 = 11.12, P < 0.01). Multiple comparisons using the Bonferroni test showed that there was a significant increment in contact frequency from the easy- to difficult-cognitive tasks and also from no cognitive task (i.e. single postural task) to difficult cognitive task conditions (p < 0.03). No significant difference was seen between the no- and easy-cognitive task conditions. For the contact time, similar results were obtained. The results of the repeated measures ANOVA showed a significant effect of cognitive loading on postural stability measures of the patients group (F2, 198 = 7.19, P < 0.01). Multiple comparisons using the Bonferroni test showed that there was a significant increment in contact time from no- to easy-cognitive tasks and also from no- to difficultcognitive task conditions (p < 0.01). No significant difference in contact time was observed between the easy- and difficult-cognitive task conditions. This pattern of change was not seen in the healthy group: there were no significant differences between the 3 levels

of cognitive difficulties for any postural stability measures (p = 0.67 and p = 0.91 for contact frequency and contact time, respectively). Moreover, the interaction of group by postural conditions was significant for both postural stability measures (F3, 144 = 3.87, P = 0.02 and F3, 144 = 3.14, P = 0.04 for contact frequency and contact time, respectively). Further analysis by independent-sample t-test showed that the patient group had higher contact frequency and longer contact time than the healthy group in all postural conditions (p < 0.02) except for the contact time during uninjured leg with straight knee condition. Also, for the contact frequency, the results of the repeated measures ANOVA showed a significant difference between 4 postural conditions of the patient group (F3, 222 = 11.37, P < 0.01). Multiple comparisons by the Bonferroni test showed a significant higher contact frequency in the inured leg compared to uninjured leg in both the straight and flexed knee conditions (p < 0.01). For the contact time, the results of the repeated measures ANOVA showed a significant difference across

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the four conditions of the patient group (F3, 222 = 6.75, P < 0.01). However, multiple comparisons by the Bonferroni test showed a non-significant difference between the injured and uninjured legs (p > 0.05). This pattern of change was not seen in the healthy group so that there were no significant differences across the four conditions for any postural stability measures (F3, 222 = 2.47, p = 0.06 and F3, 222 = 2.15, p = 0.09 for contact frequency and contact time, respectively). 3.3. Cognitive performance The mean and standard deviation (SD) of the row cognitive errors occurred in sitting, injured leg with straight knee, injured leg with flexed knee, uninjured leg with straight knee, and uninjured leg with flexed knee conditions were 0.07 ± 0.17, 0.63 ± 0.65, 0.37 ± 0.47, 0.50 ± 0.51, and 0.25 ± 0.36 for the ACLR group and 0.07 ± 0.22, 0.43 ± 0.40, 0.33 ± 0.38, 0.34 ± 0.41, and 0.34 ± 0.44 for the healthy group, respectively. The results of variance analysis showed no interaction of group by postural conditions (F4, 192 = 1.03, P = 0.39) and no main effect of group (F1, 48 = 0.53, P = 0.47), i.e. no significant difference in cognitive errors was seen between two groups. 4. Discussion The results of this study showed that with the exception of contact time during uninjured leg with straight knee, there was significantly poorer postural stability (higher contact frequency and longer contact time) in patients with ACL-R compared to healthy matched controls. More interestingly, the ACL-R patients showed decreased postural stability (higher contact frequency and longer contact time) during dual-task compared to single-task conditions. This pattern of interference was not observed in healthy control participants in whom postural stability measures remained unchanged during dual-task compared to single-task conditions. This study used the IWB to measure dynamic standing balance since it is a simple, low cost and easy to use instrument that can provide quantitative measures of postural stability for those clinicians and researchers interested in this research domain. In spite of small sample size, the results of our reliability study showed that the postural stability measures extracted from IWB were reliable outcomes to compare balance abilities between two groups of ACL-R and healthy participants. The analysis might be improved by including more participation in the future studies. Adequate maintenance of dynamic standing balance is an essential prerequisite not only for sports activities but also for most daily activities [18]. On the basis of the results obtained in this study, it appears that dynamic standing balance of patients with ACL-R was not restored to pre-injury level even after more than a year from surgery. The ACL-R group demonstrated significantly higher contact frequency and longer contact time than the healthy control group. We are not the first to report a decrease in dynamic standing balance after ACL-R surgery. Such a finding has been reported in other studies using other measures of dynamic evaluation such as BBS that showed poor balance stability during single leg stance in patients with ACL-R compared to healthy matched controls [1,7]. Briefly, the ACL tearing disrupts the postural control system through impairment in somatosensory (proprioceptive) information required for maintenance of standing balance and this deficit appears to remain several months after ACL-R surgery [6]. The results showed that concurrent execution of both postural and cognitive tasks led to performance deterioration of postural stability measures rather than cognitive measures. This pattern of posture-cognition interference suggests that the maintenance of standing balance is more attention demanding for patients with

ACL-R than healthy matched controls. Therefore, the patient group may be at a higher risk of re-injury when performing a secondary attention demanding task concurrent to dynamic balance tasks. Similar to the results obtained in this study, Rahnama et al. [14] conducted a dual-task study to investigate the attentional demands of postural control in patients with FAI while the participants were asked to maintain single leg stance on the movable BBS platform. They found decreased postural stability during dual-task compared to single-task conditions. Based on the attentional resource limitation [19], when an attention demanding cognitive task imposed on an attention demanding postural task, concurrent execution of both tasks may require more attentional capacity than the existing capacity and therefore deterioration in postural performance occurs [19]. Most activities of daily living and especially sports activities like football requires the concurrent performance of more than one task (for example maintaining standing balance while thinking about the movements of an athlete of the opposed team [14]). Therefore, information on posture-cognition interference observed for patients with ACL-R can be used to plan specific dualtask training to enhance automaticity of postural control before patients could return to pre-injury activities of sports competition. However, this recovery of function needs to be explored during the rehabilitation process. Our study was not without limitations. One is related to the contact threshold of the balance board. It was possible that during single leg stance, participants experienced relatively large excursions without contact to the floor and this may make the balance board less sensitive to minor postural deficits [13]. Also, the results of this study are only generalized to male patients who constituted all participants in the ACL-R group. In conclusion, patients who had undergone ACL-R surgery demonstrated poorer balance stability during single leg stance than healthy controls. Also, simultaneous execution of cognitive task during standing caused significant deterioration in postural stability which indicates decreased automaticity (increased attention demanding) of postural control in patients with ACL-R compared to healthy controls. Conflict of interest None. Acknowledgement Authors wish to express their special thanks to Ahvaz Jundishapur University of Medical Sciences for the financial support (Master thesis grant no: pht-9101). References [1] A.C. Alonso, J.M. Greve, G.L. Camanho, Evaluating the center of gravity of dislocations in soccer players with and without reconstruction of the anterior cruciate ligament using a balance platform, Clinics 64 (2009) 163– 170. [2] G. Andersson, J. Hagman, R. Talianzadeh, A. Svedberg, H.C. Larsen, Effect of cognitive load on postural control, Brain Res. Bull. 58 (2002) 135–139. [3] A. Field, Discovering Statistics Using SPSS, Sage Publications, London, 2005. [4] E.L. Harrison, N. Duenkel, R. Dunlop, G. Russell, Evaluation of single-leg standing following anterior cruciate ligament surgery and rehabilitation, Phys. Ther. 74 (1994) 245–252. [5] M. Henriksson, T. Ledin, L. Good, Postural control after anterior cruciate ligament reconstruction and functional rehabilitation, Am. J. Sports Med. 29 (2001) 359–366. [6] M. Hoffman, J. Schrader, D. Koceja, An investigation of postural control in postoperative anterior cruciate ligament reconstruction patients, J. Athl. Train. 34 (1999) 130–136. [7] B.E. Howells, C.L. Ardern, K.E. Webster, Is postural control restored following anterior cruciate ligament reconstruction? A systematic review, Knee Surg. Sports Traumatol. Arthrosc. 19 (2011) 1168–1177.

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Attentional demands of postural control during single leg stance in patients with anterior cruciate ligament reconstruction.

The aim of this study was to investigate the amount of attention demands of postural control in patients with anterior cruciate ligament-reconstructio...
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