Authors: Nicolas Forestier, PhD Romain Terrier, PhD Normand Teasdale, PhD
Balance
Affiliations: From the Laboratoire de Physiologie de l’Exercice EA4338, Universite´ de Savoie, France (NF, RT); CEVRES Sante´, le Bourget du Lac, France (RT); Faculte´ de Me´decine, De´partement de kine´siologie Universite´ Laval, Que´bec, Canada (NT); and Centre d’excellence sur le vieillissement de Que´bec-CHUQ, Que´bec, Canada (NT).
Correspondence: All correspondence and requests for reprints should be addressed to: Nicolas Forestier, PhD, Laboratoire de Physiologie de l’Exercice EA4338, Campus scientifique du Bourget du Lac, F73376, le Bourget du Lac, France.
Disclosures: Supported by the European Union (FEDER) and the Re´gion Rhoˆne Alpes. 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.
0894-9115/15/9401-0020 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000137
ORIGINAL RESEARCH ARTICLE
Ankle Muscular Proprioceptive Signals’ Relevance for Balance Control on Various Support Surfaces An Exploratory Study ABSTRACT Forestier N, Terrier R, Teasdale N: Ankle muscular proprioceptive signals’ relevance for balance control on various support surfaces: an exploratory study. Am J Phys Med Rehabil 2015;94:20Y27.
Objective: The purpose of this study was to test the effect of various unstable support surfaces on the relevance of muscular proprioceptive signals originating from the ankle joint.
Design: Ten healthy subjects were instructed to stand as still as possible on a force plate during 40 secs on three different surfaces: (1) stable, (2) unstableunspecific (foam), and (3) unstable-specific (inspired from rearfoot anatomy). Muscular vibration was applied on the paraspinals and fibularis muscles. The effects of vibrations on postural stability as well as fibularis longus and tibialis anterior electrical activities for each support condition were investigated.
Results: The unstable-specific support surface was associated with higher fibularis muscular activity and greater postural perturbations when fibularis muscles were vibrated than the unspecific-unstable surface.
Conclusion: Balance control on unstable-specific support surface maintains the relevance on muscular proprioceptive signals originating from ankle and increases ankle evertor muscle activity. Key Words:
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Proprioception, Ankle Sprain, Rehabilitation, Balance Control
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 1, January 2015 Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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ateral ankle sprain is one of the most frequent injuries occurring in daily life and in sport situations. It is estimated that there are more than 6,000 occurrences per day in France, which equates to one sprain per 10,000 people daily.1Y3 Clinical lateral ankle sprain rehabilitation protocols, supervised by physiotherapists, represent daily expenses of more than €1.2 million for the French collectively.4 Formal supervised rehabilitation protocols always include proprioceptive training protocols. This training allows reduced proprioceptive deficits, symptoms of giving way, risk of reinjury, and improved postural control.5 The most familiar training consists of maintaining balance in single-leg stance on a wobble board or a foam surface with and without vision. It is thought that these exercises generate multidirectional destabilization, leading the central nervous system to use proprioceptive signals from ankle mechanoreceptors for maintaining balance.6 These authors suggested that this training could promote compensation for proprioceptive deficits associated with capsulo-ligamentar lesions from other peripheral mechanoreceptors such as muscle spindles. Some studies6Y8 reported that 40%Y70% of individuals affected by an initial ankle sprain were affected by chronic ankle instability. This report also agrees with a recent meta-analysis performed to examine the effectiveness of proprioceptive exercises on the recurrence rate of ankle injuries at 12 mos.9 The main finding is that the odds ratio of recurrent ankle injury for people with or without proprioceptive training was not statistically different. These observations raise some doubts as to the effectiveness of proprioceptive training. In other words, it is not clear if using unstable surfaces (such as wobble boards or a foam surface) to rehabilitate individuals with an ankle injury leads to a greater or a better use of ankle proprioceptive information. Brumagne et al.10 have proposed a method of muscular proprioceptive disturbance based on the muscle vibration technique to examine the reliance upon proprioceptive information when standing. These authors vibrated ankle muscles (triceps surae) or back muscles (lumbar multifidus) to appraise the proprioceptive strategy of subjects who were standing on a stable or a foam surface. The foam surface presumably creates a postural condition where ankle proprioceptive signals are less relevant, therefore inducing the subject to rely on other signals for regulating balance. Kiers et al.11 also used this method to demonstrate that standing on an unstable surface does not target ankle muscle www.ajpmr.com
proprioception. Their data are consistent with results by Bernier and Perrin.12 After proprioceptive training on a multidirectional destabilization surface such as square tilt board or wobble board, these latter authors have shown an enhancement of balance control but not of proprioceptive acuity assessed with a proprioceptive matching test. In other words, training on unstable devices allows improving balance performance on the trained device, but this improvement does not seem to be mediated by an improved proprioceptive acuity. Altogether, these latter studies suggest that proprioceptive training using multidirectional and unspecific ankle destabilization generated by a foam10,11 or a wobble board13 surface may not target a greater or a better use of ankle proprioceptive inputs. Ivanenko et al.13 have proposed a hypothesis to explain why rehabilitation programs using unstable surfaces do not target ankle muscle proprioception; they suggested that the use of proprioceptive signals from the ankle was contingent upon the direction of support instability, that is, upon the specificity of the destabilization axis.14 Lateral ankle sprain results from an ankle inversion, a movement revolving about the functional axis of the subtalar joint also called Henke axis.15,16 It was hypothesized that, to target ankle muscle proprioception, the ankle destabilization should induce a movement revolving about the Henke axis. During such an ankle inversion, subtalar joint control is assumed by active (fibularis muscles) and passive (capsulo-ligamentous components) structures, which are stretched and provide proprioceptive signals and motor commands leading to active resistance to the external inversion torque acting at the ankle. The purpose of this study was to test whether, contrary to unstable-unspecific support surfaces, a specific one inspired from rearfoot functional anatomy maintains muscular proprioceptive ankle signals relevant for balance control while targeting evertor muscles activity. To this aim, the effect of muscular vibration on balance performance was analyzed when unspecific destabilization (standing on a foam surface) or specific destabilization of the rearfoot about Henke axis was used. The effect of support surface specificity on ankle muscles activity was also investigated.
EXPERIMENTAL PROCEDURE Subjects A total of 10 healthy subjects, 6 men and 4 women (age, 23.5 T 3 yrs; weight, 63.4 T 12 kg; Balance Control on Various Support Surfaces
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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vibration induced illusions are minimal with vision.19 Muscular vibration was then applied on the paraspinals or the fibularis when subjects were standing on the different support conditions. Two trials for each vibration condition (paraspinals or fibularis) for the unstable surfaces (unspecific vs. specific) were presented randomly. One trial was collected for the stable surface condition. Muscle vibration of paraspinals or fibularis was initiated about 5 secs after the start of the trial for 25 secs.
Material FIGURE 1 Illustration of the device used for the unstable-specific condition.
height, 172.7 T 5.9 cm), participated in the study. All subjects provided their written informed consent. None of the participants declared any known neurologic disorders, vestibular impairment, lower limb disorders, as well as ankle instability. The Ethical Committee of Laval University approved the protocol (ethical number 2012-278), and all procedures were applied with respect to the Declaration of Helsinki (Ethical Principles for Medical Research Involving Human Subjects).
Methods In this study, barefoot participants were asked to stay as still as possible in bipedal stance during 40 secs with their feet 10 cm apart and the arms along the body. Three different support conditions were used, and participants stood on (1) a force platform (stable), (2) a foam surface placed on the force platform (unstable-unspecific), and (3) on a force platform while equipped with an ankle destabilization device (unstable-specific). This device (Myolux Medik II, Cevres Sante´, Savoie Technolac, France) allows a forefoot stabilization (anchorage) on a stable platform while the rearfoot is destabilized by a specific articulator inducing inversion around the subtalar physiologic axis (Fig. 1).17,18 The standing task on each of the three surfaces was performed with or without vision and with or without muscular vibration applied on the paraspinal or on the fibularis muscles. Overall, data were collected for 16 trials. Subjects were instructed to look at a fixation point located on a wall facing them at 3 m. For the first six trials, subjects stood on the three different surfaces (stable, unstable-unspecific, unstable-specific) with and without vision. The last ten trials were performed without vision as it is well known that
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After the skin was shaved and cleaned to minimize skin impedance, surface electrodes (Thought Technology, Uni-Gel electrode) were placed bilaterally with a 2-cm interelectrode distance longitudinally over the bellies of the fibularis longus (FL) and the tibialis anterior (TA). Electrical (EMG) electrode placement was defined using the surface EMG for noninvasive assessment of muscles (SENIAM) guideline.20 EMG signals were preamplified close to the recording site (200) before second stage amplification (Bortec Electronics, Calgary, AB, Canada) and were recorded at a frequency of 1.2 kHz (16 bits A/D conversion). Signals were stored and transferred to a microcomputer for subsequent analyses using custom-designed computer software (Matlab, the Mathworks Inc, Natick, MA). FL and TA electrical activity associated with maximal voluntary contraction was recorded for each subject. The experimenter placed and maintained each subject’s ankle in inversion, asking the subject to replace the foot in a neutral position. Three magnetic transmitters (Polhemus Liberty) were fixed behind the subject’s head (external occipital protuberance location) and at cervical (seventh) and lumbar (fourth) regions. The position and orientation of the transmitters were recorded at 120 Hz. These data are not reported herein. The anterior-posterior and mediolateral coordinates of the center of pressure (CoP) were determined from the ground reaction force and moments recorded at 200 Hz (16-bit A/D conversion) by a force plate (AMTI model OR6-1; AMTI, Watertown, MA). To stimulate muscular proprioceptors (muscles spindles principally) similarly to the procedures presented by Brumagne et al.10 and Kiers et al.,11 two custom-made vibrators were used. For each vibrator, unbalanced masses were fixed at both extremities of a DC motor. Each motor was embedded in a plastic cylinder (10 cm long, 3 cm in diameter) and produced a mechanical oscillation of 3-mm amplitude at 100 Hz.21 The vibrators were held in
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 1, January 2015
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
TABLE 1 Mean CoP data and EMG for the three support surfaces and vibration conditions and summary of the two-way (support condition) repeated-measure ANOVAs
Variable
Support Surface
No Vibration
F Vibparaspinal
Vibfibular
Surface Vibration S V
2
Stable 0.67 T 0.43 0.99 T 0.65 2.88 T 1.47 Unstable-unspecific 10.64 T 2.30 11.93 T 4.32 9.65T 2.84 88.22a Unstable-specific 1.45 T 1.58 2.87 T 3.69 4.78 T 3.38 Stable 0.79 T 0.26 1.22 T 0.55 2.18 T 0.74 CoP speed, Unstable-unspecific 3.81 T 1.21 4.72 T 1.79 4.41 T 1.41 9.86b cm secj1 Unstable-specific 2.91 T 2.79 3.78 T 3.08 4.53 T 3.14 EMGi fibularis, Stable 8.2 T 4.6 1.7 T 8.6 8.7 T 5.4 %EMG max Unstable-unspecific 12.6 T 7.0 14.8 T 8.0 15.3 T 7.2 13.1a Unstable-specific 17.2 T 9.3 27.4 T 16.3 20.0 T 14.5 EMGi tibialis anterior, Stable 6.3 T 5.6 5.0 T 4.1 11.2 T 6.4 %EMG max Unstable-unspecific 25.4 T 25.1 27.4 T 34 37.4 T 26.2 6.02c Unstable-specific 4.1 T 2.4 6.4 T 5.1 13T 8.4
CoP surface, cm
6.67b
4.78b
23.55a
3.97b
2.42
2.21
6.17c
1.08
a
P G 0.001. P G 0.01. c P G 0.05. CoP indicates center of pressure; ANOVA, analysis of variance. b
place by means of rubber bands and positioned over the fibularis tendon (2 cm above and behind the lateral malleolus) or lumbar multifidus muscles. The activation-deactivation of the vibrators was controlled manually.
Data Reduction and Statistical Analysis The CoP data were filtered using a low-pass filter (Butterworth fourth order, 8 Hz cutoff frequency) with a dual pass to remove phase shift. To document the postural oscillations, the mean speed of the CoP and the surface covered by the CoP were calculated. The mean speed is simply the total displacement of the CoP in a given trial divided by the duration of the trial. For the surface, the ellipse containing 85% of the CoP oscillations was computed using a method proposed by Duarte and Zatsiorsky.22 For each trial, these variables were calculated for a period of 25 secs. The relative proprioceptive weighting (RPW) was appraised using the following equation for the CoP speed and the surface area: RP W ¼ðCoPVIBfibularis j CoP No VIBÞ= ½ðCoPVIBparaspinals j CoP No VIBÞ þ ðCoPVIBfibularis j CoP No VIBÞ; where (CoP No VIB), (CoPVIBfibularis), and (CoPVIBparaspinals) are the CoP speed or surface area without vibration and during fibularis and paraspinals vibrations, respectively. For both CoP speed and surface area, an RPW score of 1 correwww.ajpmr.com
sponds to an ankle proprioceptive strategy, whereas a score of 0 reveals a low back proprioceptive strategy.7 EMG signals were full wave rectified and smoothed with a weighted average moving window algorithm (25 samples). The EMG activity during the vibration period was then integrated and expressed in percentage of maximal activity. To determine if there was an adaptation across conditions for which two trials were collected, data for the postural parameters, the RPW , and the EMG activities initially were submitted to separate trial (T1 vs. T2) support surface (unspecific vs. specific) vibration condition (vibparaspinal vs. vibfibularis) analysis of variance (ANOVA) with repeated measures on all factors. The level of significance was set at P G 0.05. Data for the postural parameters and the EMG activities were compared using a support surface (stable, unstable-unspecific, unstable-specific) vibration condition (no vibration, vibparaspinal, vibfibularis) ANOVA with repeated measures on both factors. Post hoc tests (planned comparison) were performed when necessary. The level of significance was set at P G 0.05.
RESULTS For all variables, the main effect of trial and all interactions including this factor were not significant (F1,9 = 0.069, 0.047, 0.41, 0.109, and 0.59, P values 9 0.05, for the main effect of trial for CoP speed, CoP surface area, RPW, EMGFibularis, and EMGTibialis, respectively). Mean values were used for subsequent statistical analyses. Means for the Balance Control on Various Support Surfaces
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FIGURE 2 Mean and standard deviations of CoP surface area (upper panel) and speed (lower panel) for the various support surfaces and vibration conditions. Post hoc results: *P G 0.05, **P G 0.01, ***P G 0.001. CoP, center of pressure.
CoP data and muscular activities and results of the ANOVAs for the three support surfaces and vibration conditions are presented in Table 1. For both the CoP surface area and speed, the ANOVAs re-
vealed significant main effects of the surface (F2,18 = 9.86 and 88.22, P G 0.01 and 0.0001, for CoP speed and surface, respectively) and vibration (F2,18 = 23.55 and 6.72, P G 0.0001 and 0.01, for CoP surface
FIGURE 3 Mean and standard deviations of the relative proprioceptive weighting fibular/paraspinal muscles under influence of support surface and vibration calculated by mean of CoP surface area (&) or CoP speed ()) parameters. *P G 0.05, **P G 0.01, ***P G 0.001. CoP, center of pressure.
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Am. J. Phys. Med. Rehabil. & Vol. 94, No. 1, January 2015
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
FIGURE 4 Mean and standard deviations of fibularis longus (upper panel) and tibialis anterior (lower panel) electrical activities for the three support surfaces and vibration conditions (white: no vibration; grey: vibration paraspinals; black: vibration fibularis). *P G 0.05, **P G 0.01, ***P G 0.001.
area and speed, respectively) as well as a significant interaction of surface vibration condition (F4,36 = 3.97 and 4.78, P values G 0.01, for CoP surface area and speed, respectively). As illustrated in Figure 2, post hoc analyses showed that vibration of the fibularis was associated with an increased sway when subjects were standing on the stable- or the unstable-specific surfaces. For the unstableunspecific surface, however, the vibration of the fibularis did not yield an increased sway. Figure 3 presents the results for the RPW calculated for both the CoP speed and surface. For each variable, the ANOVAs revealed a main effect of surface (F2,18 = 17.88 and 21.31, P values G .001, for the RPW calculated from CoP surface area and speed, respectively). Post hoc analyses revealed that the unstable-unspecific support surface was associated with lower ratios compared with the stable and unstable-specific support surfaces (0.47 vs. 0.66 and 0.67 for the RPW calculated from CoP surface www.ajpmr.com
area; 0.48 vs. 0.7 and 0.60 for the RPW calculated from the CoP speed). The integrated EMG activity for the FL and TA are presented in Table 1 and Figure 4. For both muscles, the ANOVA yielded a main effect of the support surface (F2,18 = 13.1 and 6.02, P G 0.0001 and 0.05, for the FL and the TA, respectively). The activity of the FL was maximal for the unstablespecific support surface. On the other hand, the activity of the TA was greater for the unstableunspecific surface. The ANOVA yielded no significant interaction of surface vibration condition for EMG activities.
DISCUSSION It was hypothesized that, to target ankle muscle proprioception, the ankle destabilization should induce a movement revolving about the functional axis of the subtalar joint.15,16 Results demonstrated Balance Control on Various Support Surfaces
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that under the stable and the unstable-specific conditions the speed of the CoP and the surface area covered by the displacement of the CoP were greater when the fibularis were vibrated than when the paraspinal muscles were vibrated. The higher RPW values observed for the stable and unstable-specific supports suggest that under these conditions, balance control mostly involve ankle muscle proprioceptive signals. This result agrees with other works10,11,13 and suggests that ankle muscle proprioception is less targeted by workouts on unstableunspecific surfaces than on stable or unstable-specific surfaces. Together, these data suggest that on unspecific support surfaces, the relative gain of the proprioceptive signals from the ankle muscles is decreased in favor of proprioceptive signals from other muscles, such as the paraspinals. To test if the state of instability has directionspecific effects on the reliance of ankle muscle proprioceptive signals, Ivanenko et al.14 applied mechanical vibrations on the shank muscles in healthy subjects standing on four support conditions: (1) rigid floor, (2) movable support in the sagittal plane only, inducing anteroposterior displacements, (3) movable support in the frontal plane inducing mediolateral displacements only, and (4) hemispherical support inducing multidirectional displacements. They showed that the use of proprioceptive signals from the ankle muscles was contingent upon the destabilization axis. Postural reactions associated with mechanical vibrations were present only when subjects stood on the rigid floor and the movable support in the frontal plane. They concluded that the direction of support instability affected the processing from the ankle muscle receptors in accordance with the internal representation of the current posture. In line with the work of Ivanenko et al.,14 it was hypothesized that unstable conditions used to restore ankle muscle proprioceptive acuity have to account for the biomechanical and neurophysiologic functions of the ankle. In other words, destabilizations limited to the rearfoot and inspired from the functional mobility axis of the rearfoot should target the use of ankle muscle proprioception. Under such conditions, instability mimics the ankle sprain mechanism, and ankle muscle proprioceptive signals are prioritized by the central nervous system for balance control. The unstable-specific support used in this study allows forefoot stabilization (anchorage) on a stable platform while the rearfoot is destabilized around the subtalar physiologic axis by a specific articulator. Under such conditions, in contrast to destabilizations induced by a whole moving base such as wobble boards or foam surfaces, compression forces can be produced by the
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forefoot on the floor for posture regulation. Hence, the unstable-specific surface of the present study seems to represent the best way, from mechanical and proprioceptive viewpoints, to propose a destabilization allowing targeting of ankle muscle proprioception. Data from postural responses to vibrations and EMG activities support this hypothesis. Beyond the sensory considerations, chronic ankle instability is generally associated by welldescribed motor deficits such as fibularis muscles weakness,16,23Y25 lower evertor activation,26,27 deficits of central organization of movement,28 and corticomotor excitability of fibularis muscles.29 Together, these data support the necessity to use rehabilitation protocols requiring not only maintaining the prevalence of ankle proprioceptive signals reliance but also developing motor activity of ankle evertor muscles. In the present study, the EMG analyses clearly showed that unstable-specific condition, in comparison with the two other support conditions, leads to a specific increase in FL activity, without any significant change in TA activity. Conversely, the unstable-unspecific condition leads to large and variable increases in TA activity as well as increased FL activity. These results demonstrate that unspecific destabilizations like those generated through a foam surface do not specifically target ankle evertor muscles. In this study, the postural and EMG data clearly suggest that it is possible to design balance exercises that selectively increase ankle evertor muscles activity and, at the same time, preserve the relevance of ankle muscle proprioceptive signals for balance control. A device used to focus on both ankle sensorimotor parameters should present three main characteristics. The first is a destabilization mechanism. Indeed, although the postural effects induced by ankle vibration seem similar between the stable and the unstable-specific conditions, the instability concept seems essential for proprioceptive rehabilitation. When using unstablespecific conditions, subjects’ balance is challenged and proprioceptive compensation mechanisms are needed to deal with more complex situations than the usual one-leg balance control on a stable floor. The second characteristic concerns the rearfoot destabilization specificity, inspired from functional joint anatomy. The third mechanism is a capacity of forefoot anchorage allowing the generation of compressive ground forces for balance regulation. The results of the present study demonstrate that the relation between balance exercises and optimization of ankle muscle proprioception is not as straightforward as initially proposed by Freeman et al.6
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 1, January 2015
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REFERENCES 1. Kannus P, Renstro¨m P: Treatment for acute tears of the lateral ligaments of the ankle. Operation, cast, or early controlled mobilization. J Bone Surg Am 1991; 73:305Y12 2. Makhani JS: Diagnosis and treatment of acute rupture of the various components of the lateral ligaments of the ankle. Am J Orthop 1962;4:224Y30 3. McCulloch PB, Holden P, Robson DJ, et al: The value of mobilisation and nonsteroidal anti-inflammatory analgesia in the management of inversion injuries of the ankle. Br J Clin Pract 1985;39:69Y72 4. Bonnomet F: Les entorses de la cheville. U. L.P.Y Faculte´ de me´decine Strasbourg DCEM1YModule 12BYAppareil Loco-Moteur. Available at: http://kinefacile.e-monsite.com/medias/files/24-entorses-de-lacheville.pdf. Accessed May 5, 2014 5. Rozzi SL, Lephart SM, Sterner R, et al: Balance training for persons with functionally unstable ankles. J Orthop Sports Phys Ther 1999;29:478Y86 6. Freeman MAR, Dean MRE, Haman IWF: The etiology and prevention of functional instability of the foot. J Bone Joint Surg 1965;47:678Y85 7. Gerber JP, Williams GN, Scoville CR, et al: Persistent disability associated with ankle sprains: A prospective examination of an athletic population. Foot Ankle Int 1998;19:653Y60 8. Yeung MS, Chang KM, So CH, et al: An epidemiological survey on ankle sprain. Br J Sports Med 1994;28:112Y6 9. Postle K, Pak D, Smith TO: Effectiveness of proprioceptive exercises for ankle ligament injury in adults: A systematic literature and meta-analysis. Manual Therapy 2012;17:285Y91 10. Brumagne S, Janssens L, Knapen S, et al: Persons with recurrent low back pain exhibit a rigid postural control strategy. Eur Spine J 2008;17:1177Y84 11. Kiers H, Brumagne S, Diee¨n JV, et al: Ankle proprioception is not targeted by exercises on an unstable surface. Eur J Appl Physiol 2012;112:1577Y85 12. Bernier JN, Perrin D: Effect of coordination training on proprioception of the functionally unstable ankle. J Orthop Sports Phys Ther 1998;27:264Y75 13. Ivanenko YP, Talis VL, Kazennikov OV: Support stability influences postural responses to muscle vibration in humans. Eur J Neurosci 1999;11:647Y54 14. Ivanenko YP, Solopova IA, Levik YS: The direction of postural instability affects postural reactions to ankle muscle vibration in humans. Neurosci Lett 2000;292:103Y6 15. Fong DT, Hong Y, Shima Y, et al: Biomechanics of supination ankle sprain: A case report of an accidental
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injury event in the laboratory. Am J Sports Med 2009;37:822Y7 16. Hertel J: Functional anatomy, pathomechanics, and pathophysiology of lateral ankle instability. J Athl Train 2002;37:364Y75 17. Forestier N, Toschi P: The effect of an ankle destabilization device on muscular activity while walking. Int J Sport Med 2005;25:1Y7 18. Forestier N, Terrier R: Peroneal reaction time measurement in unipodal stance for two different destabilization axes. Clin Biomech 2011;26:766Y71 19. Lakner JR, Taulieb AB: Influence of vision on vibration-induced illusions of limb movement. Exp Neurol 1984;85:97Y106 20. Hermens HJ, Freriks B, Merletti R, et al: European recommendations for surface electromyography (SENIAM). SENIAM guidelines. Roessingh Research and Development 1999 21. Hay L, Bard C, Fleury M, et al: Availability of visual and proprioceptive afferent messages and postural control in elderly adults. Exp Brain Res 1996;108:129Y39 22. Duarte M, Zatsiorsky VM: Effects of body lean and visual information on the equilibrium maintenance during stance. Exp Brain Res 2002;146:60Y9 23. 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 24. 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 25. 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 26. Santilli V, Frascarelli MA, Paolini M, et al: Peroneus longus muscle activation pattern during gait cycle in athletes affected by functional ankle instability: A surface electromyography study. Am J Sports Med 2005;33:1183Y7 27. Suda EY, Amorim CF, Sacco Ide C: Influence of ankle functional instability on the ankle electromyography during landing after volleyball blocking. J Electromyogr Kinesiol 2009;19:84Y93 28. Hass CJ, Bishop MD, Doidge D, et al: Chronic ankle instability alters central organization of movement. Am J Sports Med 2010;38:829Y34 29. Pietrosimone BG, Gribble PA: Chronic ankle instability and corticomotor excitability of the fibularis longus muscle. J Athl Train 2012;47:621Y6
Balance Control on Various Support Surfaces Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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Balance
Affiliations: From the Laboratoire de Physiologie de l’Exercice EA4338, Universite´ de Savoie, France (NF, RT); CEVRES Sante´, le Bourget du Lac, France (RT); Faculte´ de Me´decine, De´partement de kine´siologie Universite´ Laval, Que´bec, Canada (NT); and Centre d’excellence sur le vieillissement de Que´bec-CHUQ, Que´bec, Canada (NT).
Correspondence: All correspondence and requests for reprints should be addressed to: Nicolas Forestier, PhD, Laboratoire de Physiologie de l’Exercice EA4338, Campus scientifique du Bourget du Lac, F73376, le Bourget du Lac, France.
Disclosures: Supported by the European Union (FEDER) and the Re´gion Rhoˆne Alpes. 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.
0894-9115/15/9401-0020 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000137
ORIGINAL RESEARCH ARTICLE
Ankle Muscular Proprioceptive Signals’ Relevance for Balance Control on Various Support Surfaces An Exploratory Study ABSTRACT Forestier N, Terrier R, Teasdale N: Ankle muscular proprioceptive signals’ relevance for balance control on various support surfaces: an exploratory study. Am J Phys Med Rehabil 2015;94:20Y27.
Objective: The purpose of this study was to test the effect of various unstable support surfaces on the relevance of muscular proprioceptive signals originating from the ankle joint.
Design: Ten healthy subjects were instructed to stand as still as possible on a force plate during 40 secs on three different surfaces: (1) stable, (2) unstableunspecific (foam), and (3) unstable-specific (inspired from rearfoot anatomy). Muscular vibration was applied on the paraspinals and fibularis muscles. The effects of vibrations on postural stability as well as fibularis longus and tibialis anterior electrical activities for each support condition were investigated.
Results: The unstable-specific support surface was associated with higher fibularis muscular activity and greater postural perturbations when fibularis muscles were vibrated than the unspecific-unstable surface.
Conclusion: Balance control on unstable-specific support surface maintains the relevance on muscular proprioceptive signals originating from ankle and increases ankle evertor muscle activity. Key Words:
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Proprioception, Ankle Sprain, Rehabilitation, Balance Control
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 1, January 2015 Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
L
ateral ankle sprain is one of the most frequent injuries occurring in daily life and in sport situations. It is estimated that there are more than 6,000 occurrences per day in France, which equates to one sprain per 10,000 people daily.1Y3 Clinical lateral ankle sprain rehabilitation protocols, supervised by physiotherapists, represent daily expenses of more than €1.2 million for the French collectively.4 Formal supervised rehabilitation protocols always include proprioceptive training protocols. This training allows reduced proprioceptive deficits, symptoms of giving way, risk of reinjury, and improved postural control.5 The most familiar training consists of maintaining balance in single-leg stance on a wobble board or a foam surface with and without vision. It is thought that these exercises generate multidirectional destabilization, leading the central nervous system to use proprioceptive signals from ankle mechanoreceptors for maintaining balance.6 These authors suggested that this training could promote compensation for proprioceptive deficits associated with capsulo-ligamentar lesions from other peripheral mechanoreceptors such as muscle spindles. Some studies6Y8 reported that 40%Y70% of individuals affected by an initial ankle sprain were affected by chronic ankle instability. This report also agrees with a recent meta-analysis performed to examine the effectiveness of proprioceptive exercises on the recurrence rate of ankle injuries at 12 mos.9 The main finding is that the odds ratio of recurrent ankle injury for people with or without proprioceptive training was not statistically different. These observations raise some doubts as to the effectiveness of proprioceptive training. In other words, it is not clear if using unstable surfaces (such as wobble boards or a foam surface) to rehabilitate individuals with an ankle injury leads to a greater or a better use of ankle proprioceptive information. Brumagne et al.10 have proposed a method of muscular proprioceptive disturbance based on the muscle vibration technique to examine the reliance upon proprioceptive information when standing. These authors vibrated ankle muscles (triceps surae) or back muscles (lumbar multifidus) to appraise the proprioceptive strategy of subjects who were standing on a stable or a foam surface. The foam surface presumably creates a postural condition where ankle proprioceptive signals are less relevant, therefore inducing the subject to rely on other signals for regulating balance. Kiers et al.11 also used this method to demonstrate that standing on an unstable surface does not target ankle muscle www.ajpmr.com
proprioception. Their data are consistent with results by Bernier and Perrin.12 After proprioceptive training on a multidirectional destabilization surface such as square tilt board or wobble board, these latter authors have shown an enhancement of balance control but not of proprioceptive acuity assessed with a proprioceptive matching test. In other words, training on unstable devices allows improving balance performance on the trained device, but this improvement does not seem to be mediated by an improved proprioceptive acuity. Altogether, these latter studies suggest that proprioceptive training using multidirectional and unspecific ankle destabilization generated by a foam10,11 or a wobble board13 surface may not target a greater or a better use of ankle proprioceptive inputs. Ivanenko et al.13 have proposed a hypothesis to explain why rehabilitation programs using unstable surfaces do not target ankle muscle proprioception; they suggested that the use of proprioceptive signals from the ankle was contingent upon the direction of support instability, that is, upon the specificity of the destabilization axis.14 Lateral ankle sprain results from an ankle inversion, a movement revolving about the functional axis of the subtalar joint also called Henke axis.15,16 It was hypothesized that, to target ankle muscle proprioception, the ankle destabilization should induce a movement revolving about the Henke axis. During such an ankle inversion, subtalar joint control is assumed by active (fibularis muscles) and passive (capsulo-ligamentous components) structures, which are stretched and provide proprioceptive signals and motor commands leading to active resistance to the external inversion torque acting at the ankle. The purpose of this study was to test whether, contrary to unstable-unspecific support surfaces, a specific one inspired from rearfoot functional anatomy maintains muscular proprioceptive ankle signals relevant for balance control while targeting evertor muscles activity. To this aim, the effect of muscular vibration on balance performance was analyzed when unspecific destabilization (standing on a foam surface) or specific destabilization of the rearfoot about Henke axis was used. The effect of support surface specificity on ankle muscles activity was also investigated.
EXPERIMENTAL PROCEDURE Subjects A total of 10 healthy subjects, 6 men and 4 women (age, 23.5 T 3 yrs; weight, 63.4 T 12 kg; Balance Control on Various Support Surfaces
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vibration induced illusions are minimal with vision.19 Muscular vibration was then applied on the paraspinals or the fibularis when subjects were standing on the different support conditions. Two trials for each vibration condition (paraspinals or fibularis) for the unstable surfaces (unspecific vs. specific) were presented randomly. One trial was collected for the stable surface condition. Muscle vibration of paraspinals or fibularis was initiated about 5 secs after the start of the trial for 25 secs.
Material FIGURE 1 Illustration of the device used for the unstable-specific condition.
height, 172.7 T 5.9 cm), participated in the study. All subjects provided their written informed consent. None of the participants declared any known neurologic disorders, vestibular impairment, lower limb disorders, as well as ankle instability. The Ethical Committee of Laval University approved the protocol (ethical number 2012-278), and all procedures were applied with respect to the Declaration of Helsinki (Ethical Principles for Medical Research Involving Human Subjects).
Methods In this study, barefoot participants were asked to stay as still as possible in bipedal stance during 40 secs with their feet 10 cm apart and the arms along the body. Three different support conditions were used, and participants stood on (1) a force platform (stable), (2) a foam surface placed on the force platform (unstable-unspecific), and (3) on a force platform while equipped with an ankle destabilization device (unstable-specific). This device (Myolux Medik II, Cevres Sante´, Savoie Technolac, France) allows a forefoot stabilization (anchorage) on a stable platform while the rearfoot is destabilized by a specific articulator inducing inversion around the subtalar physiologic axis (Fig. 1).17,18 The standing task on each of the three surfaces was performed with or without vision and with or without muscular vibration applied on the paraspinal or on the fibularis muscles. Overall, data were collected for 16 trials. Subjects were instructed to look at a fixation point located on a wall facing them at 3 m. For the first six trials, subjects stood on the three different surfaces (stable, unstable-unspecific, unstable-specific) with and without vision. The last ten trials were performed without vision as it is well known that
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After the skin was shaved and cleaned to minimize skin impedance, surface electrodes (Thought Technology, Uni-Gel electrode) were placed bilaterally with a 2-cm interelectrode distance longitudinally over the bellies of the fibularis longus (FL) and the tibialis anterior (TA). Electrical (EMG) electrode placement was defined using the surface EMG for noninvasive assessment of muscles (SENIAM) guideline.20 EMG signals were preamplified close to the recording site (200) before second stage amplification (Bortec Electronics, Calgary, AB, Canada) and were recorded at a frequency of 1.2 kHz (16 bits A/D conversion). Signals were stored and transferred to a microcomputer for subsequent analyses using custom-designed computer software (Matlab, the Mathworks Inc, Natick, MA). FL and TA electrical activity associated with maximal voluntary contraction was recorded for each subject. The experimenter placed and maintained each subject’s ankle in inversion, asking the subject to replace the foot in a neutral position. Three magnetic transmitters (Polhemus Liberty) were fixed behind the subject’s head (external occipital protuberance location) and at cervical (seventh) and lumbar (fourth) regions. The position and orientation of the transmitters were recorded at 120 Hz. These data are not reported herein. The anterior-posterior and mediolateral coordinates of the center of pressure (CoP) were determined from the ground reaction force and moments recorded at 200 Hz (16-bit A/D conversion) by a force plate (AMTI model OR6-1; AMTI, Watertown, MA). To stimulate muscular proprioceptors (muscles spindles principally) similarly to the procedures presented by Brumagne et al.10 and Kiers et al.,11 two custom-made vibrators were used. For each vibrator, unbalanced masses were fixed at both extremities of a DC motor. Each motor was embedded in a plastic cylinder (10 cm long, 3 cm in diameter) and produced a mechanical oscillation of 3-mm amplitude at 100 Hz.21 The vibrators were held in
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 1, January 2015
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
TABLE 1 Mean CoP data and EMG for the three support surfaces and vibration conditions and summary of the two-way (support condition) repeated-measure ANOVAs
Variable
Support Surface
No Vibration
F Vibparaspinal
Vibfibular
Surface Vibration S V
2
Stable 0.67 T 0.43 0.99 T 0.65 2.88 T 1.47 Unstable-unspecific 10.64 T 2.30 11.93 T 4.32 9.65T 2.84 88.22a Unstable-specific 1.45 T 1.58 2.87 T 3.69 4.78 T 3.38 Stable 0.79 T 0.26 1.22 T 0.55 2.18 T 0.74 CoP speed, Unstable-unspecific 3.81 T 1.21 4.72 T 1.79 4.41 T 1.41 9.86b cm secj1 Unstable-specific 2.91 T 2.79 3.78 T 3.08 4.53 T 3.14 EMGi fibularis, Stable 8.2 T 4.6 1.7 T 8.6 8.7 T 5.4 %EMG max Unstable-unspecific 12.6 T 7.0 14.8 T 8.0 15.3 T 7.2 13.1a Unstable-specific 17.2 T 9.3 27.4 T 16.3 20.0 T 14.5 EMGi tibialis anterior, Stable 6.3 T 5.6 5.0 T 4.1 11.2 T 6.4 %EMG max Unstable-unspecific 25.4 T 25.1 27.4 T 34 37.4 T 26.2 6.02c Unstable-specific 4.1 T 2.4 6.4 T 5.1 13T 8.4
CoP surface, cm
6.67b
4.78b
23.55a
3.97b
2.42
2.21
6.17c
1.08
a
P G 0.001. P G 0.01. c P G 0.05. CoP indicates center of pressure; ANOVA, analysis of variance. b
place by means of rubber bands and positioned over the fibularis tendon (2 cm above and behind the lateral malleolus) or lumbar multifidus muscles. The activation-deactivation of the vibrators was controlled manually.
Data Reduction and Statistical Analysis The CoP data were filtered using a low-pass filter (Butterworth fourth order, 8 Hz cutoff frequency) with a dual pass to remove phase shift. To document the postural oscillations, the mean speed of the CoP and the surface covered by the CoP were calculated. The mean speed is simply the total displacement of the CoP in a given trial divided by the duration of the trial. For the surface, the ellipse containing 85% of the CoP oscillations was computed using a method proposed by Duarte and Zatsiorsky.22 For each trial, these variables were calculated for a period of 25 secs. The relative proprioceptive weighting (RPW) was appraised using the following equation for the CoP speed and the surface area: RP W ¼ðCoPVIBfibularis j CoP No VIBÞ= ½ðCoPVIBparaspinals j CoP No VIBÞ þ ðCoPVIBfibularis j CoP No VIBÞ; where (CoP No VIB), (CoPVIBfibularis), and (CoPVIBparaspinals) are the CoP speed or surface area without vibration and during fibularis and paraspinals vibrations, respectively. For both CoP speed and surface area, an RPW score of 1 correwww.ajpmr.com
sponds to an ankle proprioceptive strategy, whereas a score of 0 reveals a low back proprioceptive strategy.7 EMG signals were full wave rectified and smoothed with a weighted average moving window algorithm (25 samples). The EMG activity during the vibration period was then integrated and expressed in percentage of maximal activity. To determine if there was an adaptation across conditions for which two trials were collected, data for the postural parameters, the RPW , and the EMG activities initially were submitted to separate trial (T1 vs. T2) support surface (unspecific vs. specific) vibration condition (vibparaspinal vs. vibfibularis) analysis of variance (ANOVA) with repeated measures on all factors. The level of significance was set at P G 0.05. Data for the postural parameters and the EMG activities were compared using a support surface (stable, unstable-unspecific, unstable-specific) vibration condition (no vibration, vibparaspinal, vibfibularis) ANOVA with repeated measures on both factors. Post hoc tests (planned comparison) were performed when necessary. The level of significance was set at P G 0.05.
RESULTS For all variables, the main effect of trial and all interactions including this factor were not significant (F1,9 = 0.069, 0.047, 0.41, 0.109, and 0.59, P values 9 0.05, for the main effect of trial for CoP speed, CoP surface area, RPW, EMGFibularis, and EMGTibialis, respectively). Mean values were used for subsequent statistical analyses. Means for the Balance Control on Various Support Surfaces
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FIGURE 2 Mean and standard deviations of CoP surface area (upper panel) and speed (lower panel) for the various support surfaces and vibration conditions. Post hoc results: *P G 0.05, **P G 0.01, ***P G 0.001. CoP, center of pressure.
CoP data and muscular activities and results of the ANOVAs for the three support surfaces and vibration conditions are presented in Table 1. For both the CoP surface area and speed, the ANOVAs re-
vealed significant main effects of the surface (F2,18 = 9.86 and 88.22, P G 0.01 and 0.0001, for CoP speed and surface, respectively) and vibration (F2,18 = 23.55 and 6.72, P G 0.0001 and 0.01, for CoP surface
FIGURE 3 Mean and standard deviations of the relative proprioceptive weighting fibular/paraspinal muscles under influence of support surface and vibration calculated by mean of CoP surface area (&) or CoP speed ()) parameters. *P G 0.05, **P G 0.01, ***P G 0.001. CoP, center of pressure.
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Am. J. Phys. Med. Rehabil. & Vol. 94, No. 1, January 2015
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
FIGURE 4 Mean and standard deviations of fibularis longus (upper panel) and tibialis anterior (lower panel) electrical activities for the three support surfaces and vibration conditions (white: no vibration; grey: vibration paraspinals; black: vibration fibularis). *P G 0.05, **P G 0.01, ***P G 0.001.
area and speed, respectively) as well as a significant interaction of surface vibration condition (F4,36 = 3.97 and 4.78, P values G 0.01, for CoP surface area and speed, respectively). As illustrated in Figure 2, post hoc analyses showed that vibration of the fibularis was associated with an increased sway when subjects were standing on the stable- or the unstable-specific surfaces. For the unstableunspecific surface, however, the vibration of the fibularis did not yield an increased sway. Figure 3 presents the results for the RPW calculated for both the CoP speed and surface. For each variable, the ANOVAs revealed a main effect of surface (F2,18 = 17.88 and 21.31, P values G .001, for the RPW calculated from CoP surface area and speed, respectively). Post hoc analyses revealed that the unstable-unspecific support surface was associated with lower ratios compared with the stable and unstable-specific support surfaces (0.47 vs. 0.66 and 0.67 for the RPW calculated from CoP surface www.ajpmr.com
area; 0.48 vs. 0.7 and 0.60 for the RPW calculated from the CoP speed). The integrated EMG activity for the FL and TA are presented in Table 1 and Figure 4. For both muscles, the ANOVA yielded a main effect of the support surface (F2,18 = 13.1 and 6.02, P G 0.0001 and 0.05, for the FL and the TA, respectively). The activity of the FL was maximal for the unstablespecific support surface. On the other hand, the activity of the TA was greater for the unstableunspecific surface. The ANOVA yielded no significant interaction of surface vibration condition for EMG activities.
DISCUSSION It was hypothesized that, to target ankle muscle proprioception, the ankle destabilization should induce a movement revolving about the functional axis of the subtalar joint.15,16 Results demonstrated Balance Control on Various Support Surfaces
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that under the stable and the unstable-specific conditions the speed of the CoP and the surface area covered by the displacement of the CoP were greater when the fibularis were vibrated than when the paraspinal muscles were vibrated. The higher RPW values observed for the stable and unstable-specific supports suggest that under these conditions, balance control mostly involve ankle muscle proprioceptive signals. This result agrees with other works10,11,13 and suggests that ankle muscle proprioception is less targeted by workouts on unstableunspecific surfaces than on stable or unstable-specific surfaces. Together, these data suggest that on unspecific support surfaces, the relative gain of the proprioceptive signals from the ankle muscles is decreased in favor of proprioceptive signals from other muscles, such as the paraspinals. To test if the state of instability has directionspecific effects on the reliance of ankle muscle proprioceptive signals, Ivanenko et al.14 applied mechanical vibrations on the shank muscles in healthy subjects standing on four support conditions: (1) rigid floor, (2) movable support in the sagittal plane only, inducing anteroposterior displacements, (3) movable support in the frontal plane inducing mediolateral displacements only, and (4) hemispherical support inducing multidirectional displacements. They showed that the use of proprioceptive signals from the ankle muscles was contingent upon the destabilization axis. Postural reactions associated with mechanical vibrations were present only when subjects stood on the rigid floor and the movable support in the frontal plane. They concluded that the direction of support instability affected the processing from the ankle muscle receptors in accordance with the internal representation of the current posture. In line with the work of Ivanenko et al.,14 it was hypothesized that unstable conditions used to restore ankle muscle proprioceptive acuity have to account for the biomechanical and neurophysiologic functions of the ankle. In other words, destabilizations limited to the rearfoot and inspired from the functional mobility axis of the rearfoot should target the use of ankle muscle proprioception. Under such conditions, instability mimics the ankle sprain mechanism, and ankle muscle proprioceptive signals are prioritized by the central nervous system for balance control. The unstable-specific support used in this study allows forefoot stabilization (anchorage) on a stable platform while the rearfoot is destabilized around the subtalar physiologic axis by a specific articulator. Under such conditions, in contrast to destabilizations induced by a whole moving base such as wobble boards or foam surfaces, compression forces can be produced by the
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forefoot on the floor for posture regulation. Hence, the unstable-specific surface of the present study seems to represent the best way, from mechanical and proprioceptive viewpoints, to propose a destabilization allowing targeting of ankle muscle proprioception. Data from postural responses to vibrations and EMG activities support this hypothesis. Beyond the sensory considerations, chronic ankle instability is generally associated by welldescribed motor deficits such as fibularis muscles weakness,16,23Y25 lower evertor activation,26,27 deficits of central organization of movement,28 and corticomotor excitability of fibularis muscles.29 Together, these data support the necessity to use rehabilitation protocols requiring not only maintaining the prevalence of ankle proprioceptive signals reliance but also developing motor activity of ankle evertor muscles. In the present study, the EMG analyses clearly showed that unstable-specific condition, in comparison with the two other support conditions, leads to a specific increase in FL activity, without any significant change in TA activity. Conversely, the unstable-unspecific condition leads to large and variable increases in TA activity as well as increased FL activity. These results demonstrate that unspecific destabilizations like those generated through a foam surface do not specifically target ankle evertor muscles. In this study, the postural and EMG data clearly suggest that it is possible to design balance exercises that selectively increase ankle evertor muscles activity and, at the same time, preserve the relevance of ankle muscle proprioceptive signals for balance control. A device used to focus on both ankle sensorimotor parameters should present three main characteristics. The first is a destabilization mechanism. Indeed, although the postural effects induced by ankle vibration seem similar between the stable and the unstable-specific conditions, the instability concept seems essential for proprioceptive rehabilitation. When using unstablespecific conditions, subjects’ balance is challenged and proprioceptive compensation mechanisms are needed to deal with more complex situations than the usual one-leg balance control on a stable floor. The second characteristic concerns the rearfoot destabilization specificity, inspired from functional joint anatomy. The third mechanism is a capacity of forefoot anchorage allowing the generation of compressive ground forces for balance regulation. The results of the present study demonstrate that the relation between balance exercises and optimization of ankle muscle proprioception is not as straightforward as initially proposed by Freeman et al.6
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REFERENCES 1. Kannus P, Renstro¨m P: Treatment for acute tears of the lateral ligaments of the ankle. Operation, cast, or early controlled mobilization. J Bone Surg Am 1991; 73:305Y12 2. Makhani JS: Diagnosis and treatment of acute rupture of the various components of the lateral ligaments of the ankle. Am J Orthop 1962;4:224Y30 3. McCulloch PB, Holden P, Robson DJ, et al: The value of mobilisation and nonsteroidal anti-inflammatory analgesia in the management of inversion injuries of the ankle. Br J Clin Pract 1985;39:69Y72 4. Bonnomet F: Les entorses de la cheville. U. L.P.Y Faculte´ de me´decine Strasbourg DCEM1YModule 12BYAppareil Loco-Moteur. Available at: http://kinefacile.e-monsite.com/medias/files/24-entorses-de-lacheville.pdf. Accessed May 5, 2014 5. Rozzi SL, Lephart SM, Sterner R, et al: Balance training for persons with functionally unstable ankles. J Orthop Sports Phys Ther 1999;29:478Y86 6. Freeman MAR, Dean MRE, Haman IWF: The etiology and prevention of functional instability of the foot. J Bone Joint Surg 1965;47:678Y85 7. Gerber JP, Williams GN, Scoville CR, et al: Persistent disability associated with ankle sprains: A prospective examination of an athletic population. Foot Ankle Int 1998;19:653Y60 8. Yeung MS, Chang KM, So CH, et al: An epidemiological survey on ankle sprain. Br J Sports Med 1994;28:112Y6 9. Postle K, Pak D, Smith TO: Effectiveness of proprioceptive exercises for ankle ligament injury in adults: A systematic literature and meta-analysis. Manual Therapy 2012;17:285Y91 10. Brumagne S, Janssens L, Knapen S, et al: Persons with recurrent low back pain exhibit a rigid postural control strategy. Eur Spine J 2008;17:1177Y84 11. Kiers H, Brumagne S, Diee¨n JV, et al: Ankle proprioception is not targeted by exercises on an unstable surface. Eur J Appl Physiol 2012;112:1577Y85 12. Bernier JN, Perrin D: Effect of coordination training on proprioception of the functionally unstable ankle. J Orthop Sports Phys Ther 1998;27:264Y75 13. Ivanenko YP, Talis VL, Kazennikov OV: Support stability influences postural responses to muscle vibration in humans. Eur J Neurosci 1999;11:647Y54 14. Ivanenko YP, Solopova IA, Levik YS: The direction of postural instability affects postural reactions to ankle muscle vibration in humans. Neurosci Lett 2000;292:103Y6 15. Fong DT, Hong Y, Shima Y, et al: Biomechanics of supination ankle sprain: A case report of an accidental
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injury event in the laboratory. Am J Sports Med 2009;37:822Y7 16. Hertel J: Functional anatomy, pathomechanics, and pathophysiology of lateral ankle instability. J Athl Train 2002;37:364Y75 17. Forestier N, Toschi P: The effect of an ankle destabilization device on muscular activity while walking. Int J Sport Med 2005;25:1Y7 18. Forestier N, Terrier R: Peroneal reaction time measurement in unipodal stance for two different destabilization axes. Clin Biomech 2011;26:766Y71 19. Lakner JR, Taulieb AB: Influence of vision on vibration-induced illusions of limb movement. Exp Neurol 1984;85:97Y106 20. Hermens HJ, Freriks B, Merletti R, et al: European recommendations for surface electromyography (SENIAM). SENIAM guidelines. Roessingh Research and Development 1999 21. Hay L, Bard C, Fleury M, et al: Availability of visual and proprioceptive afferent messages and postural control in elderly adults. Exp Brain Res 1996;108:129Y39 22. Duarte M, Zatsiorsky VM: Effects of body lean and visual information on the equilibrium maintenance during stance. Exp Brain Res 2002;146:60Y9 23. 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 24. 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 25. 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 26. Santilli V, Frascarelli MA, Paolini M, et al: Peroneus longus muscle activation pattern during gait cycle in athletes affected by functional ankle instability: A surface electromyography study. Am J Sports Med 2005;33:1183Y7 27. Suda EY, Amorim CF, Sacco Ide C: Influence of ankle functional instability on the ankle electromyography during landing after volleyball blocking. J Electromyogr Kinesiol 2009;19:84Y93 28. Hass CJ, Bishop MD, Doidge D, et al: Chronic ankle instability alters central organization of movement. Am J Sports Med 2010;38:829Y34 29. Pietrosimone BG, Gribble PA: Chronic ankle instability and corticomotor excitability of the fibularis longus muscle. J Athl Train 2012;47:621Y6
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