Eccentric Training Improves Ankle Evertor and ...

Authors: Erdal Hanci, MD Ufuk Sekir, MD Hakan Gur, MD, PhD Bedrettin Akova, MD

Sports Medicine

Affiliations: From the Department of Sports Medicine, Bursa Sevket Yilmaz Education and Research Hospital, Bursa, Turkey (EH); and Department of Sports Medicine, Medical Faculty of Uludag University, Bursa, Turkey (US, HG, BA).

Correspondence: All correspondence and requests for reprints should be addressed to: Ufuk Sekir, MD, Department of Sports Medicine, Medical Faculty of Uludag University, 16059 Gorukle, Bursa, Turkey.

Disclosures: This manuscript was edited for grammar, spelling, vocabulary, and phrasing by the American Journal Experts. Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.

ORIGINAL RESEARCH ARTICLE

Eccentric Training Improves Ankle Evertor and Dorsiflexor Strength and Proprioception in Functionally Unstable Ankles ABSTRACT Hanci E, Sekir U, Gur H, Akova B: Eccentric training improves ankle evertor and dorsiflexor strength and proprioception in functionally unstable ankles. Am J Phys Med Rehabil 2016;95:448Y458.

Objective: The aim of this study was to investigate the effects of a combined eccentric-concentric exercise program of the ankle evertors and dorsiflexors on proprioception in functionally unstable ankles. Design: Thirteen male recreational athletes with unilateral functional ankle

0894-9115/16/9506-0448 American Journal of Physical Medicine & Rehabilitation Copyright * 2016 Wolters Kluwer Health, Inc. All rights reserved.

instability were admitted to this study. The unaffected opposite ankles were used as controls. The functionnaly unstable ankle of the subjects performed an isokinetic exercise program of the ankle evertors and dorsiflexors in a combined eccentric-concentric mode for 3 days per week for 6 wks. Before and after the isokinetic exercise program, active and passive joint position sense and kinesthesia and isokinetic strength of the ankle joint were evaluated.

DOI: 10.1097/PHM.0000000000000421

Results: Active and passive joint position sense error scores for inversion (P G 0.01Y0.001) and plantarflexion (P G 0.05Y0.001) direction and kinesthesia scores for inversion (P G 0.001) and plantarlexion (P G 0.01) direction showed significant reductions after 6 wks of intervention in the functionnaly unstable ankle. In addition, eccentric peak torques for the ankle evertor and dorsiflexors represented significant (P G 0.001) increases in the functionnaly unstable ankle compared with the control ankle.

Conclusions: The results of this study suggest that it is possible to improve proprioceptive acuity of the ankle joint after a 6-wk eccentric-concentric isokinetic training program in functionally unstable ankles. Key Words: Instability

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Eccentric Exercise, Proprioception, Muscle Strength, Functional Ankle

Am. J. Phys. Med. Rehabil. & Vol. 95, No. 6, June 2016 Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.

I

nversion sprains of the lateral ankle ligaments are one of the most common injuries in athletes.1 Almost 40% of those who experience inversion sprains experience residual disability, referred to as functional ankle instability (FAI).2 Sensorimotor deficits, including impaired proprioception3 and weakness of the ankle muscles,4Y6 have been suggested as potential causes of FAI. Although there is strong evidence for decreased proprioceptive abilities in patients with functionally unstable ankles,7 the evidence for decreased muscle strength is inconclusive, with several studies reporting muscle weakness4,8 but other studies finding no differences in the ankle invertor and/or evertor muscles.6,9 Dynamic support through eccentric muscle actions provided from both the peroneal and tibialis anterior muscles is one of the key components in the prevention of a lateral ankle sprain when the ankle is forced into plantar flexion/inversion.4,5 Therefore, eccentric strengthening exercises of the ankle evertors and even the dorsiflexors seem to be important to be able to resist an inversion sprain. It can be hypothesized that lengthening contractions of the muscles via eccentric strength training might enhance the firing of the static gamma motor neurons, thereby altering muscle spindle sensitivity and leading to decreases in inversion trauma. Accordingly, researchers have already demonstrated eccentric evertor weakness in patients with FAI.4,5,8,10,11 Willems et al.5 hypothesized that the weakness and slow reaction of the ankle evertor muscles would directly reduce the effective protection of the ankle joint from inversion trauma. Nevertheless, in addition to increases in muscle strength, improvements in proprioceptive ability after strengthening of the ankle evertor muscles either with an isokinetic concentric intervention6 or with progressive resistance strength training using Theraband elasticated bands (Thera-Band Tubing Resistive Exerciser, The Hygenic Corporation, Akron, OH)12 have also been reported in several studies. These improvements have been attributed to enhancements in muscle spindle activity.6,12 These findings suggest that strength training without an emphasis on proprioception may be beneficial in improving both strength and proprioception deficits. At the same time, although eccentric exercises are recommended for ankle rehabilitation,8,10,11,13 there is limited information in the literature about the effects of eccentric ankle exercise programs on strength and proprioceptive measures in functionally unstable ankles. Two studies, one in healthy14 and the other in first-time ankle-sprained subjects,15 investigated the www.ajpmr.com

effects of eccentric training. They reported significant improvements in ankle strength and/or peroneal reaction time. Thus, the aim of this study was to determine the effects of combined eccentric-concentric training of the ankle muscles on proprioception and strength in individuals with functionally unstable ankles. The isokinetic system was selected for this study to facilitate an accurate standardization of the eccentric-concentric exercise program.

MATERIALS AND METHODS Subjects A total of 13 male recreational athletes with unilateral FAI participated in this study (Table 1). Participants and procedure flow through the study are described in Figure 1. Of the 13 subjects, 10 experienced symptoms of unilateral ankle instability of their dominant limb and 3 experienced such symptoms in their nondominant limb. Because previous work has demonstrated no significant strength differences for inversion and eversion movements between dominant and non-dominant limbs,16 the unaffected opposite ankles were used as controls (CONT ankle) in the present study. According to the recommendations of the International Ankle Consortium,17 subjects were included in the study if they had sustained at least two moderate sprains to the same ankle that required medical intervention and if they complained of repeated episodes of Bgiving way,[ both within the last 6 mos. All patients were examined by the same clinician using the anterior drawer and talar tilt test and were found to have no mechanical instability before participating. A moderate sprain was defined as the presence of moderate pain, swelling, and tenderness over the involved ligaments without a significant instability (a definite endpoint was present on ligamentous testing). No subjects had experiences injury to the contralateral healthy ankles for at least 6 mos before testing, and none of them were undergoing rehabilitation of the injured ankle before initiating the test TABLE 1 Subject demographics and characteristics Mean T SD Age, years Weight, kg Height, cm Body mass index, kg/m2

26.1 T 73.9 T 175.4 T 24 T

5.2 7.3 6.8 1.5

Range 18Y36 62Y87 162Y187 21.7Y26.3

Eccentric Training and Proprioception Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.

449

FIGURE 1 Flow diagram of participants.

procedure, nor did they have any complaints of pain, swelling, or functional limitations in the injured ankles during the test period. Based on a comparison with the opposite healthy ankle joint, the active range of motion (dorsiflexion/plantarflexion; inversion/eversion) as measured using an electronic goniometer (Cybex EDI-320, Ronkonkoma, NY) was found to be within normal limits in the injured ankle joint for all subjects. No subjects were involved in physical activity that exceeded three sessions a week of more than half an hour per session. Written consent was obtained from each subject before testing, and all subjects were screened to ensure that there were no lower-extremity neuromuscular or musculoskeletal problems or contraindications for isokinetic testing. After being informed of the study and test procedures and any possible risks and discomfort that might ensue, all subjects read and signed an informed consent form that had been approved by the university_s Institutional Ethical Board for Protection of Human Subjects, which also approved the study.

Experimental Procedure Before and after the isokinetic exercise program, all testing protocols were performed on two separate days. The proprioceptive ability of the ankle joint was tested on the first day. On the

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second day, the isokinetic strength of the ankle joint was evaluated.

Proprioceptive Ability of the Ankle Joint Measurements of active and passive joint position sense and kinesthesia were used to evaluate the proprioceptive ability of the ankle joint.

Ankle Joint Position Sense The ankle joint position sense was measured using a computerized isokinetic dynamometer (Cybex NORM, CSMI) at a 0.5 degrees/sec angular speed. To evaluate active and passive ankle joint position senses, 10 and 20 degrees of ankle inversion and 15 and 30 degrees of ankle plantarflexion were selected as the test angles. The tested foot was placed on the footplate of the Cybex according to the manufacturer_s instructions for isolating inversion/ eversion and plantarflexion/dorsiflexion and was secured using Velcro straps. Before testing, the Cybex dynamometer was calibrated as part of the regular schedule for maintaining the equipment used for this testing device. To initiate the test, the foot was placed in the neutral (0 degrees) position. All of the participants were blindfolded to eliminate the contribution of visual cues and used foam earplugs to eliminate auditory cues during the repositioning of the joint.


For familiarization with the testing device, participants were instructed to perform three active repetitions of ankle movements. The movements ranged from maximal ankle inversion to maximal eversion for the inversion/eversion direction and from maximal ankle plantarflexion to maximal dorsiflexion for the plantarflexion/dorsiflexion direction. The test began with the tester passively moving the tested ankle into the testing position at 10 degrees of inversion or 15 degrees of plantarflexion and maintaining that position for 5 secs. After 5 secs of static positioning, the ankle was moved back passively from the presented angle to the reference angle (neutral position). Thereafter, the participant was asked to actively reproduce the previously presented test angle of 10 degrees of inversion or 15 degrees of plantarflexion at 0.5 degrees/sec angular speed, signaling to the tester when he thought the test angle had been reached. Three trials were performed. After the first test angle, the same testing protocol was used for 20 degrees of inversion or 30 degrees of plantarflexion relative to the starting angle (neutral position). After completing the active joint position sense testing, the same testing procedure was repeated to reproduce the testing angles passively. Angular displacement was recorded as the error in degrees between the reference angle and the repositioned test angle. The overestimated or underestimated angular displacements from the reference angle were not considered in calculating the error scores. Thus, only the absolute errors were noted. The mean of three trials for each tested condition was calculated to determine the average absolute error for the scores.

Kinesthesia Kinesthesia is evaluated by determining the threshold for detecting passive motion in the joint and was measured using the continuous passive motion mode of the isokinetic dynamometer (Cybex NORM, CSMI) at an angular speed of 0.1 degrees/sec. The participant positioning on the isokinetic dynamometer_s platform used in the measurements of sensitivity to joint position was used in this test as well. To initiate the test, the foot was placed in the neutral (0 degrees) position. After the participants were blindfolded, wore the foam earplugs, and were ready for testing, the dynamometer began to move continuously from the neutral position to inversion or plantarflexion at an angular speed of 0.1 degrees/sec at any time over a period of 1 min. The participants were asked to identify passive motion or a change www.ajpmr.com

in joint position. If they felt any motion, they were told to signal the tester. Three trials were performed. The threshold for detecting passive motion was determined as the error in degrees between the starting angle (neutral position) and the angle where the subject detected passive motion. The mean of the three trials for each tested condition was calculated to determine the average error of the scores.

Isokinetic Strength Measurement A detailed description of the same isokinetic strength measurement protocol used in this study has been published previously by Keles et al.14 In brief, isokinetic testing of the ankle evertor and dorsiflexor muscles was performed at velocities of 60, 180, and 300 degrees/sec for eccentric and concentric contractions of the dominant ankle using the isokinetic dynamometer (Cybex NORM, CSMI). Eventually, the highest force moment (torque) from five maximal concentric and eccentric evertor or dorsiflexor trials was taken to determine the peak torque (PT) value.

Combined Eccentric-Concentric Isokinetic Exercise Protocol To accurately standardize the exercise program, the isokinetic system was preferred for the study. In addition, combined eccentric-concentric training was chosen for the study (1) to be able to exercise only the ankle evertors or dorsiflexors without the contribution of their antagonist muscles and (2) because the contraction of these muscles is initially eccentric and subsequently concentric during a sudden ankle inversion moment as observed for the most common ankle sprain, that is, inversion sprain.18 The Cybex NORM isokinetic system was used for the isokinetic exercise program. The subjects performed the isokinetic exercise in the inversion/ eversion movement pattern to exercise the ankle evertors. When the isokinetic dynamometer moved from the neutral position to eversion, the evertors contracted concentrically; thereafter, when the isokinetic dynamometer moved from eversion to the neutral position, the evertors contracted eccentrically. After 5 mins of rest, the exercise in the plantarflexion/dorsiflexion movement pattern was performed to exercise the ankle dorsiflexors. As in the case of the evertor muscles, when the isokinetic dynamometer moved from the neutral position to dorsiflexion, the dorsiflexors contracted concentrically, and thereafter, when the isokinetic dynamometer Eccentric Training and Proprioception

Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.

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moved from dorsiflexion to the neutral position, the dorsiflexors contracted eccentrically. Each exercise session was performed using one set of six repetitions at 60, 120, 180, 240, and 300 degrees/sec. These sessions were repeated three times per week and lasted 6 wks. During this period, the control side (ankle) of the subjects did not perform any specific exercise.

Data Analysis Statistical analysis was performed with SPSS version 16.0 (SPSS, SPSS Inc, Chicago, IL) software. The mean, the standard error of the mean, and 95% confidence intervals were used to describe all variables. All tests were two tailed, and the level of significance was set at P G 0.05. A repeatedmeasures 2 (group/side) 2 (time) analysis of variance (ANOVA) model was used for comparisons of changes in strength and proprioception parameters in both the exercise and control conditions. If an appropriate and significant interaction was indicated, follow-up analyses included a paired-samples t test to examine the difference between preintervention and postintervention within the two groups. In addition, a one-way ANOVA model was used to determine the statistical significance of the difference between the two groups_ pretest mean scores. To evaluate the percentage change values between the baseline value and the value after 6 wks, the formula (%Change) = [(postintervention j preintervention)/ preintervention) 100] was used. A power analysis was performed based on the reported values of the study (PASS 13 Power Analysis and Sample Size Software; NCSS, LLC, Kaysville, UT). According to the analysis for repeated-measures design, group sample sizes of n1 = n2 = 13 achieved an effect standard deviation of 1.79 (an effect size

of 0.86) and 98% power for strength values of the ankle evertor muscles, an effect standard deviation of 1.23 (an effect size of 0.62) and 86% power for strength values of the ankle dorsiflexor muscles, an effect standard deviation of 0.31 (an effect size of 1.2) and 99% power for joint position sense values in the inversion direction, an effect standard deviation of 0.50 (an effect size of 0.82) and 97% power for joint position sense values in the plantarflexion direction, and an effect standard deviation of 0.05 (an effect size of 0.76) and 96% power for kinesthesia values, all with a significance level (alpha) of 0.05.

RESULTS Isokinetic Strength Ankle Evertor Muscles Table 2 presents the mean PT values, including concentric and eccentric strength, in the CONT ankle and FAI ankle for the evertor muscles. There were no statistically significant differences between the pretest scores for both sides of the ankles for evertor PT values (P 9 0.05). According to the 2 2 ANOVA model, the PT for the ankle evertor muscles showed a significant group (side) time interaction for the concentric mode at an angular velocity of 180 degrees/sec (F1, 24 = 4.48, P = 0.046) and for the eccentric modes at angular velocities of 60 degrees/sec (F1, 24 = 24.66, P = 0.000045), 180 degrees/sec (F1, 24 = 32.78, P = 0.000007), and 300 degrees/sec (F1, 24 = 17.20, P = 0.00036). No significant group (side) time effects were observed for the concentric modes at 60 degrees/sec (F1, 24 = 1.16, P = 0.292) and 300 degrees/sec (F1, 24 = 0.00, P = 1.000). In addition to the nonsignificant differences in the CONT

TABLE 2 Muscle strength values of the ankle evertor muscles at 60, 180, and 300 degrees/sec angular velocities in the functionally unstable and healthy ankles before and after the exercise intervention FAI

Con60PT, Nm Con180PT, Nm Con300PT, Nm Ecc60PT, Nm Ecc180PT, Nm Ecc300PT, Nm

P

CONT

Before

After

Before

After

(Group Time)

22.6 T 1.2 (20.0Y25.3) 16.8 T 0.9 (14.9Y18.6) 16.9 T 0.9 (14.9Y19.0) 29.9 T 1.8 (25.9Y33.8) 30.3 T 1.5 (27.1Y33.6) 30.9 T 1.6 (27.5Y34.4)

26.2 T 1.6 (23.6Y29.7) 19.9 T 1.1a (17.2Y22.6) 16.8 T 0.9 (14.9Y18.6) 37.9 T 1.5b (34.6Y41.1) 37.5 T 1.3b (34.8Y40.3) 37.8 T 1.6b (34.4Y41.2)

21.1 T 1.3 (18.3Y23.9) 17.3 T 1.2 (14.9Y19.6) 16.9 T 1.1 (14.5Y19.2) 32.9 T 1.7 (29.2Y36.6) 33.5 T 2.0 (29.1Y37.8) 31.8 T 2.5 (26.4Y37.2)

22.6 T 1.2 (20.0Y25.3) 17.4 T 0.9 (15.3Y19.6) 16.7 T 0.9 (14.7Y18.7) 33.8 T 2.0 (29.5Y38.0) 34.3 T 2.1 (29.7Y39.0) 33.0 T 2.3 (28.0Y38.0)

90.05 G0.05 90.05 G0.001 G0.001 G0.001

Data are presented as mean T SEM (95% confidence interval). Ecc indicates eccentric; Con, concentric; Nm, Newton-meter. a P G 0.05 (after exercise). b P G 0.001 (after exercise).

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TABLE 3 Muscle strength values of the ankle dorsiflexor muscles at 60, 180, and 300 degrees/sec angular velocities in the functionally unstable and healthy ankles before and after the exercise intervention FAI Before Con60PT, Nm Con180PT, Nm Con300PT, Nm Ecc60PT, Nm Ecc180PT, Nm Ecc300PT, Nm

After

22.5 T 1.5 (19.3Y25.8) 18.2 T 0.9 (16.3Y20.2) 17.3 T 0.6 (16.0Y18.7) 48.2 T 2.2 (43.4Y53.0) 49.4 T 2.2 (44.6Y54.2) 47.5 T 2.0 (43.2Y51.9)

P

CONT

a

28.0 T 1.6 (24.6Y31.4) 21.1 T 0.8 (19.3Y22.9) 18.5 T 0.8 (16.7Y20.3) 57.5 T 2.2b (52.7Y62.2) 56.5 T 2.8b (50.4Y62.8) 53.8 T 2.4b (48.6Y59.0)

Before

After

(Group Time)

24.2 T 1.8 (20.3Y28.2) 18.6 T 1.5 (15.4Y21.8) 16.7 T 0.9 (14.7Y18.7) 51.2 T 1.9 (46.9Y55.4) 50.5 T 2.1 (46.1Y55.0) 52.2 T 2.4 (47.0Y57.5)

24.8 T 1.4 (21.7Y27.9) 18.9 T 1.1 (16.4Y21.3) 17.3 T 0.5 (16.1Y18.5) 53.9 T 1.9 (49.8Y58.1) 51.3 T 2.1 (46.7Y55.9) 52.2 T 2.2 (47.5Y56.8)

G0.05 90.05 90.05 G0.001 G0.001 G0.001

Data are presented as mean T SEM (95% confidence interval). Ecc indicates Eccentric; Con, Concentric; Nm, Newton-meter. a P G 0.01 (after exercise). b P G 0.001 (after exercise).

ankle (P 9 0.05), a follow-up analysis for the FAI ankle showed significant increases in the evertor muscles for the concentric mode at 180 degrees/sec (P = 0.019, 19%) and for the eccentric modes at all three angular velocities (P = 0.000007 for 60 degrees/sec, 27%; P = 0.000001 for 180 degrees/sec, 24%; and P = 0.000019 for 300 degrees/sec, 22%).

Ankle Dorsiflexor Muscles Table 3 presents the mean PT values, including concentric and eccentric strength, on both sides of the ankles for the dorsiflexor muscles. There were no statistically significant differences between the pretest scores for both sides of the ankles for the dorsiflexor PT values (P 9 0.05). In addition, the PT for the ankle dorsiflexor muscles showed a significant group (side) time interaction for the concentric mode at 60 degrees/sec (F1, 24 = 7.00, P = 0.014) and for the eccentric modes at 60 degrees/sec (F1, 24 = 32.84, P = 0.000007),

180 degrees/sec (F1, 24 = 27.18, P = 0.000024), and 300 degrees/sec (F1, 24 = 20.88, P = 0.000124). No significant group (side) time effects were observed for the concentric modes at 180 degrees/sec (F1, 24 = 3.92, P = 0.059) and 300 degrees/sec (F1, 24 = 0.18, P = 0.677) velocities. In contrast with the nonsignificant differences for the CONT ankle (P 9 0.05), a follow-up analysis of the FAI ankle showed significant increases in the dorsiflexor muscles for the concentric mode at 60 degrees/sec (P = 0.007, 24%) and for the eccentric modes at all three angular velocities (P = 0.000001 for 60 degrees/sec, 19%; P = 0.000002 for 180 degrees/sec, 14%; and P = 0.000094 for 300 degrees/sec, 13%).

Proprioceptive Ability Ankle Joint Position Sense Tables 4 and 5 present the mean values for the ankle joint position sense error scores in the two groups of ankles during passive and active

TABLE 4 Joint position sense in the inversion direction in the functionally unstable and healthy ankles before and after the exercise intervention

Before

After

Before

After

P (Group Time)

3.4 T 0.3a (2.8Y4.1) 2.4 T 0.2a (1.9Y2.9) 3.2 T 0.3d (2.5Y3.9) 2.8 T 0.3d (2.2Y3.4)

2.2 T 0.2b (1.8Y2.6) 1.5 T 0.2c (1.1Y1.9) 1.9 T 0.2b (1.5Y2.4) 1.6 T 0.2c (1.2Y2.1)

2.2 T 0.2 (1.7Y2.7) 1.5 T 0.2 (1.1Y1.9) 1.6 T 0.2 (1.1Y2.0) 1.4 T 0.2 (1.0Y1.8)

2.2 T 0.2 (1.8Y2.6) 1.4 T 0.2 (1.1Y1.8) 1.6 T 0.2 (1.2Y2.0) 1.5 T 0.2 (1.2Y1.9)

G0.01 G0.001 G0.01 G0.001

FAI

PasInv20, degrees PasInv10, degrees ActInv20, degrees ActInv10, degrees

CONT

Data are presented as mean T SEM (95% confidence interval). Pas indicates passive; Act, active; Inv, inversion; 10, 10 degrees of inversion; 20, 20 degrees of inversion. a P G 0.01 (between unstable and healthy ankle). b P G 0.01 (after exercise). c P G 0.001 (after exercise). d P G 0.001 (between unstable and healthy ankle).

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TABLE 5 Joint position sense in the plantarflexion direction in the functionally unstable and healthy ankles before and after the exercise intervention

Before

After

Before

After

P (Group Time)

a

b

3.3 T 0.3 (2.7Y3.9) 1.9 T 0.2 (1.4Y2.5) 2.7 T 0.3 (2.1Y3.4) 2.2 T 0.3 (1.6Y2.8)

3.2 T 0.3 (2.6Y3.7) 1.8 T 0.2 (1.5Y2.1) 3.0 T 0.4 (2.1Y3.9) 1.9 T 0.2 (1.4Y2.4)

G0.01 G0.05 G0.001 90.05

FAI

PasPF30, degrees PasPF15, degrees ActPF30, degrees ActPF15, degrees

5.7 T 0.5 (4.7Y6.7) 3.0 T 0.2c (2.4Y3.5) 5.4 T 0.6c (4.1Y6.7) 3.0 T 0.4 (2.2Y3.9)

CONT

3.6 T 0.4 (2.8Y4.4) 2.3 T 0.2b (1.8Y2.7) 3.1 T 0.3b (2.5Y3.7) 2.0 T 0.3 (1.3Y2.8)

Data are presented as mean T SEM (95% confidence interval). Pas indicates passive; Act, active; PF, plantarflexion; 15, 15 degrees of plantarflexion; 30, 30 degrees of plantarflexion. a P G 0.001 (between unstable and healthy ankle). b P G 0.001 (after exercise). c P G 0.01 (between unstable and healthy ankle).

test modes for the inversion and plantarflexion direction, respectively. Except for a nonsignificant difference in the joint position sense error score measured actively at 15 degrees plantarflexion (P 9 0.05), all the other joint position sense test values, both in the inversion and plantarflexion directions, showed statistically significant differences among the two ankle groups_ pretest scores (P G 0.05Y0.01). Based on the 2 2 ANOVA model, except for the active joint position sense measurement at 15-degree plantarflexion (F1, 24 = 3.48, P = 0.075), the joint position sense error scores in the inversion and plantarflexion direction exhibited a significant group (side) time interaction (F1, 24 = 14.54, P = 0.001 for passive joint position sense at 20-degree inversion; F1, 24 = 22.71, P = 0.000075 for passive joint position sense at 10-degree inversion; F1, 24 = 14.01, P = 0.001 for active joint position sense at 20-degree inversion; F1, 24 = 23.48, P = 0.000061 for active joint position sense at 10-degree inversion; F1, 24 = 15.50, P = 0.001 for passive joint position sense at 30-degree plantarflexion; F1, 24 = 4.86, P = 0.037 for passive joint position sense at 15-degree plantarflexion; and F1, 24 = 16.40, P = 0.000465 for active joint position sense at 30-degree

plantarflexion). Although the active joint position sense measurement at 15-degree plantarflexion did not display any significant change (P 9 0.05), a follow-up analysis indicated significant improvements for the passive joint position sense at 10 degrees (P G 0.001, 38%) and 20 degrees (P G 0.01, 35%) of inversion, 15 degrees (P G 0.001, 23%) and 30 degrees (P G 0.001, 37%) of plantarflexion, and active joint position sense at 10 degrees (P G 0.001, 43%) and 20 degrees (P G 0.01, 41%) of inversion, and 30 degrees of plantarflexion (P G 0.001, 43%) in the FAI ankle.

Kinesthesia The joint position sense test scores showed that the threshold for detecting passive motion, both in the inversion and plantarflexion directions, differed significantly between the CONT and FAI ankles for the pretest measurements (P G 0.01, Table 6). According to the 2 2 ANOVA model, the threshold to detect passive motion scores in the inversion (F1, 24 = 21.76, P = 0.000097) and plantarflexion (F1, 24 = 12.66, P = 0.002) direction showed a significant group (side) time interaction.

TABLE 6 Kinesthesia in the inversion and plantarflexion directions in the functionally unstable and healthy ankles before and after the exercise intervention

Before

After

Before

After

P (Group Time)

a

b

0.5 T 0.1 (0.5Y0.6) 0.5 T 0.1 (0.5Y0.6)

0.6 T 0.1 (0.5Y0.6) 0.5 T 0.1 (0.5Y0.6)

G0.001 G0.01

FAI

KinInv, degrees KinPF, degrees

0.7 T 0.1 (0.6Y0.8) 0.8 T 0.1a (0.6Y0.9)

CONT

0.5 T 0.1 (0.4Y0.6) 0.6 T 0.1b (0.5Y0.6)

Data are presented as mean T SEM (95% confidence interval). Kin indicates kinesthesia; Inv, inversion; PF, plantarflexion. a P G 0.01 (between unstable and healthy ankle). b P G 0.01 (after exercise).

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A follow-up analysis indicated significant improvements in these test values (P G 0.01Y0.001; 29% for inversion and 25% for plantarflexion) only in the FAI ankle.

DISCUSSION The main purpose of this study was to investigate whether a 6-wk isokinetic eccentric-concentric exercise intervention would affect muscle strength and proprioception in FAI. It was also hypothesized that proprioceptive acuity, in addition to ankle strength, could be improved by the program used in the study. Factors such as ligament laxity, proprioceptive impairment, balance instability, and strength deficit (especially in the case of the ankle evertors) have been hypothesized as potential causes of FAI,4,5,19Y21 and ankle muscle weakness is the most questionable factor.19 The analysis of eccentric strength in this study, as in previous studies comparing the evertor strength of the functionally unstable ankle with that of the contrary uninjured limb,6,9 also did not show muscle weakness in subjects with unilateral FAI compared with the contrary healthy ankle. Furthermore, whereas all the available studies of eccentric dorsiflexor strength in FAI used healthy matched controls and reported no deficits,10,21 no eccentric dorsiflexor strength deficits in functionally unstable ankles compared with the contrary uninjured limb were found in this study. However, proprioceptive acuity was significantly decreased in the functionally unstable ankles. Results similar to this have been found by the previous studies that also compared functionally unstable ankles with the contrary healthy ankles.6,22Y24 In addition, joint position sense and kinesthesia test values attained levels similar to those of the CONT ankle after the isokinetic eccentric-concentric exercise. In view of these results, it can be concluded that proprioceptive acuity could be restored by the isokinetic exercise used in this study.

Eccentric Exercise Effects Although studies of muscle strength in FAI have been inconclusive to date, strengthening exercises for the ankle muscles have been recommended in rehabilitation programs.20 Given that repetitive ankle joint injuries cause neurosensory, proprioceptive, and muscle strength impairment, exercises that increase proprioception are also routinely performed in addition to strengthening of the ankle musculature. An ideal exercise program should improve www.ajpmr.com

not only muscle strength but also proprioceptive ability. Therefore, by investigating how strength training may improve both strength and proprioception at the same time, clinicians may allow patients to decrease treatment time and return to participation more rapidly.12 Because lateral ankle sprain occurs when the ankle is forced into plantarflexion/inversion, eccentric activity of the ankle dorsiflexor and evertor muscle groups is necessary to prevent this injury.4,5,25 Therefore, eccentric strengthening exercises of the ankle evertors and even the dorsiflexors seem to be important to be able to resist an inversion sprain. With the exception of one study that incorporated an isokinetic concentric intervention,6 most studies that investigated the effects of exercise interventions on both strength and proprioceptive ability used various isotonic exercises, such as progressive-resistance-rubber-tubing strengthening exercises of the ankle evertor and/or invertor muscles, in patients with FAI.12,26Y30 However, the results of these studies were inconsistent. Hale et al.27 and Lee et al.29 investigated comprehensive rehabilitation programs that addressed range of motion, strength, and neuromuscular control. These two studies found increases in ankle strength and balance scores in terms of Star Excursion Balance Test results. In contrast, Smith et al.30 and Docherty et al.12 focused on a single 6-wk anklestrengthening program using exercise bands made of rubber tubing and examined the effects of the program on proprioception and strength development in subjects with functionally unstable ankles. Docherty et al.12 found that ankle eversion isometric strength values and inversion joint position error scores improved by almost 46% and 59%, respectively, whereas only an increase in ankle isometric eversion strength by approximately 55%, with no improvements in proprioception as measured by force sense, was observed by Smith et al.30 In addition, Sekir et al.6 found significant increases in isokinetic concentric ankle eversion strength (11%) and significant improvements in ankle joint position sense (29%Y43%) after isokinetic concentric strengthening exercise of the ankle evertor and invertor muscles in patients with FAI. However, other studies have not demonstrated similar improvements in strength and/or proprioceptive ability after isotonic exercise, such as progressiveresistance-rubber-tubing strengthening exercises of the ankle evertor and/or invertor muscles, in patients with FAI.26,28 Kaminski et al.26 performed a progressive resistance protocol with Thera-band elasticated bands on the ankle muscles of functionally unstable ankles and reported no improvements Eccentric Training and Proprioception

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in ankle eversion-to-inversion isokinetic strength ratios (concentric eversion/eccentric inversion) after a 6-wk strength training protocol. It was stated that the protocol that was initiated with the lowerresistance Thera-bands used in the protocol might not have provided sufficient resistance to challenge the ankle muscles and improve strength. Han and Ricard28 sought to quantify the rehabilitative training effect of 4 wks of training with elastic-resistance exercise on ankle evertor strength and proprioceptive ability evaluated with peroneal reflex response time in subjects with a history of ankle sprain. Similarly, 4 wks of elastic-tubing exercise did not elicit any change in one-repetition-maximum ankle evertor strength and reflex latency. Although the peroneal muscles initially contract eccentrically when the ankle is forced into inversion,4 none of the abovementioned studies used eccentric strengthening or investigated its effects. The same considerations also apply to the ankle dorsiflexor muscles because lateral ankle sprains occur primarily when the ankle is in the plantarflexion position. Despite the importance of eccentric strength and strengthening in opposing inversion sprain,8,10,11,13,21 only a few studies have concentrated on eccentric strengthening exercises of the ankle evertor and plantarflexor muscles.14,15 Collado et al.15 investigated the effectiveness of eccentric reinforcement of the ankle evertors with the help of a physiotherapist in subjects having a first episode of ankle sprain. When the foot of the subjects was blocked in the eversion position, the physiotherapist manually pushed the foot inward, and the subject had to resist the imposed inversion movement. After 1 mo of treatment, the isokinetic eccentric strength of the injured evertor muscles increased significantly and became even stronger than on the healthy side. The authors concluded that eccentric reinforcement is a valuable method for restoring strength. In a previous study conducted in the authors_ laboratory, Keles et al.14 demonstrated improvements both in eccentric evertor and dorsiflexor strength and proprioceptive ability measured with peroneal and tibialis anterior latency time after eccentric training of ankle evertor and dorsiflexors. However, the subjects who participated in the study were all healthy subjects. The increases in eccentric strength of the ankle evertor and dorsiflexor muscles were 19% to 58% and 16% to 24%, respectively. The authors stated that these results confirmed the effectiveness of their eccentric exercise training for gaining strength and proprioception in healthy ankles. In the current study, it was also found that a similar 6-wk combined eccentric-concentric isokinetic exercise program

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had positive effects on the strength of the ankle muscles and on proprioceptive ability evaluated with joint position sense and kinesthesia in functionally unstable ankles. The eccentric strength of the ankle evertor and dorsiflexors increased by 22% to 27% and 13% to 19%, respectively; joint position sense for inversion and plantarflexion direction improved by 35% to 43% and 23% to 43%, respectively; and kinesthesia during inversion and plantarflexion direction improved by 29% and 25%, respectively. These results confirm the effectiveness of the evaluated exercise training for facilitating strength and proprioception gains in functionally unstable ankles.

Eccentric Strengthening and Improvements in Proprioceptive Acuity There could be possible links between the increases in eccentric muscle strength and improvements in afferent pathways (joint position sense and kinesthesia) related to proprioceptive acuity. It is known that in addition to input from afferents arising from the ligament and joint capsule, there is also input from proprioceptive receptors located in the cutaneous, muscle (muscle spindle) and tendon (Golgi tendon organ) tissues. The improvement, or decrease in error scores, could be attributed to enhancements in muscle spindle sensitivity and gamma motor/efferent activation after gaining eccentric strength in the muscles.6,12 The muscle spindles are stretch receptors and receive stimuli from static and dynamic gamma motor neurons. Their functions are to furnish information about sustained and/or instantaneous spindle length (static response) and the rate of length changes (dynamic response).31 Gamma motor neurons innervate the intrafusal fibers of the muscle spindle. When stimulated, they can adjust the sensitivity of these intrafusal fibers and enhance afferent responses.31 Because joint position sense and kinesthesia are tested at low velocities (0.1Y0.5 degrees/sec), it is possible that lengthening or stretching of the evertor and dorsiflexor muscles via eccentric muscle contractions might increase the amount of static gamma motor neuron activity to the spindles of these muscles. Consequently, the spindle may be more sensitive to sustained or instantaneous stretch and show better acuity in sensing joint position and kinesthesia. It can be hypothesized that the increased sensitivity of the muscle spindles because of the eccentric component of the current strength training might have produced the increase in proprioceptive acuity. However, because it was not objectively evaluated in the present


study, the possible existence of this mechanism is only speculative.

4. Hartsell HD, Spaulding SJ: Eccentric/concentric ratios at selected velocities for the invertor and evertor muscles of the chronically unstable ankle. Br J Sports Med 1999;33:255Y8

CONCLUSIONS

5. Willems T, Witvrouw E, Verstuyft J, et al: Proprioception and muscle strength in subjects with a history of ankle sprains and chronic instability. J Athl Train 2002;37:487Y93

The results of the present study demonstrated improvements in proprioceptive acuity even with only a strengthening exercise program. Similar results have been observed previously in other studies.6,12,14 Hereby, it can be concluded that the 6-wk eccentric-concentric isokinetic exercise program used in this study can significantly improve proprioceptive acuity, in addition to improving ankle muscle strength in subjects with functionally unstable ankles. In addition, further studies to test the hypothesis that including eccentric exercises in an isotonic exercise program could be similar in effectiveness to the present isokinetic program might also enhance current knowledge of ankle sprains.

Study Limitations One of the limitations of the present study is that the subjects did not wear headphones to eliminate auditory cues during ankle joint position sense and kinesthesia measurements. Instead of wearing headphones, foam earplugs were used to keep out noises in this study. Although earplugs are sufficient in a particular extent, using headphones would be better to eliminate auditory cues. Another limitation of this study is that the relationship between increases in strength and improvements in sensory neurons, which are related to proprioception, after eccentric strengthening exercise was not objectively evaluated. Only some hypothetical and speculative links were provided in the discussion. Therefore, further investigations on the effect of eccentric muscle activity and the response of muscle spindles and/or gamma motor and sensory neurons would be appropriate to explain the mechanisms. REFERENCES 1. Fong DT, Hong Y, Chan LK, et al: A systematic review on ankle injury and ankle sprain in sports. Sports Med 2007;37:73Y94 2. Safran MR, Benedetti RS, Bartolozzi AR, et al: Lateral ankle sprains: A comprehensive review. Part 1: Etiology, pathoanatomy, histopathogenesis, and diagnosis. Med Sci Sports Exerc 1999;31:S429Y37 3. Konradsen L, Beynnon BD, Renstrom PA: Proprioception and sensorimotor control in the functionally unstable ankle, in: Lephart SM, Fu FH (eds): Proprioception and Neuromuscular Control in Joint Stability. Champaign, IL: Human Kinetics, 2000, pp. 238Y9 www.ajpmr.com

6. Sekir U, Yildiz Y, Hazneci B, et al: Effect of isokinetic training on strength, functionality and proprioception in athletes with functional ankle instability. Knee Surg Sports Traumatol Arthrosc 2007;15:654Y64 7. Fu AS, Hui-Chan CW: Ankle joint proprioception and postural control in basketball players with bilateral ankle sprains. Am J Sports Med 2005;33: 1174Y82 8. Yildiz Y, Aydin T, Sekir U, et al: Peak and end range eccentric evertor/concentric invertor muscle strength ratios in chronically unstable ankles: Comparison with healthy individuals. J Sports Sci Med 2003; 2:70Y6 9. Munn J, Beard DJ, Refshauge KM, et al: Eccentric muscle strength in functional ankle instability. Med Sci Sports Exerc 2003;35:245Y50 10. Abdel-Aziem AA, Draz AH: Functionally unstable ankle effect on eccentric peak torque at two different angular velocitites. Bull Fac Ph Th Cairo Univ 2010;15:61Y7 11. David P, Halimi M, Mora I, et al: Isokinetic testing of evertor and invertor muscles in patients with chronic ankle instability. J Appl Biomech 2013;29: 696Y704 12. Docherty CL, Moore JH, Arnold BL: Effects of strength training on strength development and joint position sense in functionally unstable ankles. J Athl Train 1998;33:310Y4 13. Negahban H, Moradi-Bousari A, Naghibi S, et al: The eccentric torque production capacity of the ankle, knee, and hip muscle groups in patients with unilateral chronic ankle instability. Asian J Sports Med 2013;4:144Y52 14. Keles SB, Sekir U, Gur H, et al: Eccentric/concentric training of ankle evertor and dorsiflexors in recreational athletes: Muscle latency and strength. Scand J Med Sci Sports 2014;24:e29Y38 15. Collado H, Coudreuse JM, Graziani F, et al: Eccentric reinforcement of the ankle evertor muscles after lateral ankle sprain. Scand J Med Sci Sports 2010; 20:241Y6 16. Lin WH, Liu YF, Hsieh CC, et al: Ankle eversion to inversion strength ratio and static balance control in the dominant and non-dominant limbs of young adults. J Sci Med Sport 2009;12:42Y9 17. Gribble PA, Delahunt E, Bleakley C, et al: Selection criteria for patients with chronic ankle instability in controlled research. A position statement of the International Ankle Consortium. Br J Sports Med 2014; 48:1014Y8


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18. Vaes P, Duquet W, Van Gheluwe B: Peroneal reaction times and eversion motor response in healthy and unstable ankles. J Athl Train 2002;37:475Y80 19. Kaminski TW, Perrin DH, Gansneder BM: Eversion strength analysis of uninjured and functionally unstable ankles. J Athl Train 1999;34:239Y45 20. Kaminski TW, Hartsell HD: Factors contributing to chronic ankle instability: A strength perspective. J Athl Train 2002;37:394Y405 21. Fox J, Docherty CL, Schrader J, et al: Eccentric plantar-flexor torque deficits in participants with functional ankle instability. J Athl Train 2008;43:51Y4 22. Garn SN, Newton RA: Kinesthetic awareness in subjects with multiple ankle sprains. Phys Ther 1988; 68:1667Y71 23. Nakasa T, Fukuhara K, Adachi N, et al: The deficit of joint position sense in the chronic unstable ankle as measured by inversion angle replication error. Arch Orthop Trauma Surg 2008;128:445Y9 24. Witchalls J, Waddington G, Blanch P, et al: Ankle instability effects on joint position sense when stepping across the active movement extent discrimination apparatus. J Athl Train 2012;47:627Y34 25. Bernier JN, Perrin DH, Rijke A: Effect of unilateral functional instability of the ankle on postural sway

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and inversion and eversion strength. J Athl Train 1997;32:226Y32 26. Kaminski TW, Buckley BD, Powers ME, et al: Effect of strength and proprioception training on eversion to inversion strength ratios in subjects with unilateral functional ankle instability. Br J Sports Med 2003;37:410Y5 27. Hale SA, Hertel J, Olmsted-Kramer LC: The effect of a four week comprehensive rehabilitation program on postural control and lower extremity function in individuals with chronic ankle instability. J Orthop Sports Phys Ther 2007;37:303Y11 28. Han KM, Ricard MD: Effects of 4 weeks of elasticresistance training on ankle-evertor strength and latency. J Sport Rehabil 2011;20:157Y73 29. Lee KY, Lee HJ, Kim SE, et al: Short term rehabilitation and ankle instability. Int J Sports Med 2012; 33:485Y96 30. Smith BI, Docherty CL, Simon J, et al: Ankle strength and force sense after a progressive, 6-week strengthtraining program in people with functional ankle instability. J Athl Train 2012;47:282Y8 31. Kandel ER, Schwartz JH, Lessell TM: Spinal reflexes, in: Buttler J, Leowitz H, (eds): Principles of Neural Science. ed 4. New York, NY: McGraw-Hill, 2000, pp. 713Y36
