The relationship between ankle joint physiological characteristics and balance control during unilateral stance

Gait & Posture 39 (2014) 718–722

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The relationship between ankle joint physiological characteristics and balance control during unilateral stance Daniel J. Amin a,*, Lee C. Herrington b,1 a

Centre for Human Performance, Department of Sport, Fitness and Exercise Science, School of Humanities, Education, Sport and Social Sciences, University Centre Doncaster, Doncaster DN1 2JR, United Kingdom b Directorate of Sport, Exercise and Physiotherapy, School of Healthcare Professionals, University of Salford, Salford M5 4WT, United Kingdom

A R T I C L E I N F O

A B S T R A C T

Article history: Received 25 February 2013 Received in revised form 23 June 2013 Accepted 2 October 2013

Background: The role that the ankle’s physiological characteristics play in maintaining balance during quiet stance has been well documented. However, the role of the ankle in maintaining balance during more challenging conditions is questionable. As such, the objectives of this study were to identify any significant relationships between the physiological characteristics of the ankle joint and the ability to maintain more challenging unilateral stance. Participants: 21 healthy, adult athletes (age = 24.67  5.42 years; height = 175.34  7.48 cms; weight = 79.09  14.07 kg). Procedures: Passive resistance and joint position sense in the sagittal plane of the ankle, and active dorsiflexion range of motion of each subject was assessed, in addition to centre of pressure parameters during 20 s unilateral stance. Results: Pearson’s product moment correlation coefficient found significant positive correlations between Dpeak torque and sway area (r = .554); Ax range (r = .449); and Ay range (r = .471). Significant negative correlations were found between Ppeak torque angle and sway area (r = .538, p = .012), Ax range (r = .590, p = .005) and Ay range (r = .439, p = .046). Discussion: The results highlighted limited relationships between unilateral stance balance control and the ankle characteristics commonly associated with quiet stance balance control and has, thus, further questioned the role that the ankle plays during more challenging stance conditions. The majority of balance training protocols in the athletic community focuses on the distal joints, however, this needs readdressing in order to maximise performance. ß 2013 Elsevier B.V. All rights reserved.

Keywords: Inverted pendulum Stability Passive resistance Flexibility Proprioception

1. Introduction Balance is the ability of the human body to maintain the position of its centre of gravity (COG) within the area of its base of support (BOS). If the COG is displaced out of the BOS, the body becomes unbalanced, senses this threat to stability and uses muscular activity to counteract the force of gravity in order to prevent falling [1]. Thus, a balance control system, which involves both the central and peripheral nervous systems constantly interacting, needs to be activated in order for stability to be maintained [2]. Decreased balance control has been associated with higher injury risk in sport [3] and can explain differences

* Corresponding author. Tel.: +44 1302553585. E-mail addresses: [email protected] (D.J. Amin), [email protected] (L.C. Herrington). 1 Tel.: +44 1612952326. 0966-6362/$ – see front matter ß 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2013.10.004

between individuals with and without functional ankle instability (FAI) [4]. In unperturbed, bilateral (‘‘quiet’’) stance, the body has been considered as an inverted pendulum whereby the balance control system must contend with gravity as the largest destabilising force [5] and chooses patterns that require a minimal number of muscles [6]. It has been demonstrated that ankle mechanisms dominate in the sagittal plane with an almost synchronous sway of the body parts [7], and emphasises the theory of the ‘‘ankle strategy’’ as the balance control system during quiet stance [8]. Some of the physiological characteristics of the ankle in the sagittal plane, which have received consideration when trying to understand the ankle-strategy’s role in quiet stance balance control, have included stiffness (passive resistance; PR), proprioception and flexibility [9]. However, both an ankle and a ‘‘hip strategy’’ have been described in more perturbed situations [10]. It has been suggested that during situations more challenging than quiet stance, the sways are too great for the ankle to act and, as such, the hip would

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respond to flex, thus moving COG posteriorly, or to extend to move the COG anteriorly [8]. However, research is still sparse when considering this strategy in challenging balance conditions. This is an important issue in sport as an athlete often undergoes situations of perturbed stance, for instance when coming into contact with an opponent, and unilateral stance conditions during all forms of locomotion, jumping, landing and striking an object with the foot. So it seems important to know what physiological contributing factors may be present that influence balance control during more challenging stance conditions. The objectives of this study were to identify if any associations existed between stiffness, flexibility or proprioception of the ankle in the sagittal plane, and balance control during unilateral stance. The significance of this is to ascertain whether the ankle strategy has an influence during a stance more challenging and more common in the sporting realm than quiet stance or whether balance control can be attributed to other proposed mechanisms, thus potentially influencing future balance training protocols. 2. Methodology 2.1. Participants Twenty-one university athletes (n = 12, males; n = 9, females; age = 24.67  5.42 years; height = 175.34  7.48 cm; weight = 79.09  14.07 kg) competing within their respective sports, as part of the national university league, volunteered to participate in the study. All subjects gave their informed consent and the study was approved by the institute’s review board and Ethics Committee. Subjects were assessed for suitability through a written questionnaire and those meeting any of the exclusion criteria featured in Table 1 were removed from the study. 2.2. Procedures Participants undertook 4 separate tests, within one testing session. The tests attempted to ascertain the following physiological parameters: stiffness, in the form of PR in the sagittal plane of the ankle joint; flexibility, in the form of active range of motion (AROM) in the sagittal plane of the ankle joint; proprioception, in the form of joint position sense (JPS) in the sagittal plane of the ankle joint; and balance control, in the form of centre of pressure (COP) parameters during unilateral stance. Due to the geographical location of the testing bays, the tests were not counterbalanced. The time between each test and their relatively distinct nature was deemed appropriate to minimise confounding effects; however, the authors are aware that these effects may still have been present. The right leg was assessed for each subject as differences between proposed dominant and non-dominant legs have not been found for these parameters [11]. Three trials for each test were administered in order to ascertain a mean value from which to use for data analysis. 2.3. Stiffness assessment A fully calibrated KinCom AP2 isokinetic dynamometer (Chattanooga Group Inc.; California, USA; 1997) was used to measure PR during ankle dorsiflexion and plantarflexion in order to determine a measure of PR at 58/s [12]. The angular range that the dynamometer took the ankle joint through was within 58 of subjective end-range dorsiflexion and plantarflexion. The primary investigator ensured participants sat with right knee fully extended [13], as this mimicked the unilateral stance condition, with the upper part of the right leg firmly secured to the dynamometer seat in order to limit any knee movement during the trials. The left leg was allowed to hang over the edge of the seat of

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Table 1 Participant exclusion criteria. Current lower limb musculoskeletal injury Incidence of minor head injury within the previous 6 months Lower limb orthopaedic conditions, including a history of chronic ankle instability Impairment of the visual system that could not be rectified with spectacles or contact lenses Impairments of the vestibular system Neurological conditions, which have a noticeable effect on tactile sensation Any athlete who undergoes balance training as part of their training regimen

the dynamometer, flexed at the knee joint, parallel to the right leg, whilst the dynamometer passively moved the ankle joint through dorsiflexion until end range, then through to plantarflexion end range, with the maximum peak torque values being recorded during each trial (‘Dpeak torque’ and ‘Ppeak torque’, Nm) [14]. Torque and angular position (8) on the KinCom were sampled with a frequency of 100 Hz and data was transferred using the Shelton KinCom Data Transfer Programme v1.0.28 (Shelton Technical Ltd.; Milton Keynes, UK) to a Windows XP SP3 computer (Viglen Genie, 3.0 GHz Duo processor, 2GB Ram). The values for peak torque were normalised based on the angular displacement that occurred during the trials [15] (‘Dpeak torque angle’ and ‘Ppeak torque angle’, Nm/ 8). 2.4. Flexibility assessment Participants were asked to actively dorsiflex their ankle to its end range before relaxing to their neutral position. The primary investigator ensured participants lay supine on a fixed massage couch with their right knee extended and foot hanging over the edge of the couch [16]. Markers were placed at the lateral malleolus, head of 5th metatarsal and mid-way between head of fibular and lateral malleolus. Their left leg was flexed to 458 at the hip and 908 at the knee; so as to mimic the unilateral stance condition. Participants were then asked to actively dorsiflex their ankle to its end range before relaxing to their neutral position [16]. 2-D motion analysis was chosen to assess maximal AROM in dorsiflexion (‘AROM’,8) as it has low measurement error [17]. A Casio Exilim EX-FH25 high-speed camera (Casio Inc.; New Jersey, USA) was positioned level with the axis of rotation, in the sagittal plane, 1 m from the lateral malleolus and recorded all trials at 100 frames per second. Quintic Biomechanics v21 software (Quintic Consultancy Ltd.; Coventry, UK) was then used by the primary investigator to identify maximal AROM in dorsiflexion. 2.5. Proprioception assessment The ipsilateral angle reproduction test used was ‘‘passive production, active reproduction’’ [18] which involved the active reproduction of a passively specified target position. The difference between the target position and the subject’s estimated target position was the outcome measure, irrespective of directional difference, and was known as absolute error (AE). The participants were positioned by the primary investigator in a similar manner to the AROM measures, with the anatomical markers in the same locations and the Casio Exilim EX-FH25 high-speed camera located in the same place. The ankle was passively dorsiflexed from the relaxed starting position to a set, pre-determined target position and the participant was informed of this by the primary investigator using the word ‘‘target’’. The ankle remained in this position for 5 s and was then passively moved to full plantarflexion and returned to the starting position. After remaining in the starting position for 3 s, the participant was asked, through use of the word ‘‘reproduce’’, to actively move their ankle in an attempt to match the target position. When the participant considered the

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to concentrate on, 2 m directly ahead of the force platform and 1.7 m high to ensure a consistent approach, with each trial lasting 20 s [19]. 3. Data analysis

Fig. 1. Unilateral stance undertaken during balance control assessment.

ankle to be at the target position, they spoke the word ‘‘yes’’ [18]. Quintic Biomechanics v21 software was again used by the primary investigator to assess ‘JPS AE’ (8). 2.6. Balance control assessment A Kistler 9286AA portable force platform (Kistler Instrumente AG; Winterthur, Switzerland) based on piezoelectrical measurement of ground-reaction force in the sagittal and frontal planes was used to collect COP data. COP signals were sampled at 50 Hz and filtered with a sixth-order Butterworth zero-phase low-pass filter at 10 Hz. The COP parameters measured were total sway area (‘sway area’, cm2) and sway range in the sagittal (‘Ax range’, mm) and frontal (‘Ay range’, mm) planes. Fig. 1 shows the unilateral stance undertaken by each participant. An eyes-open condition was selected in order to try and mimic real-life settings, and the participants were provided with a fixed marker

All statistical analyses were conducted using SPSS for Windows version 16.0 (SPSS Inc., Chicago, IL). Alpha levels were set at .05 for all tests. Based on the mean values from the 3 trials, Pearson’s product moment correlation coefficient was used to determine any relationships between the testing variables. Any independent variables proposed to have an influence on balance control, based on the literature (PR, AROM or JPS measures [9]) that correlated significantly with a ‘dependent’ variable (sway area, Ax range or Ay range) underwent bivariate and standard multiple regression analyses, using an enter methodology, to determine what level of the particular dependent variable’s variance could be predicted by the independent variables [20]. The following assumptions were considered for the regression analyses [20]: ratio of participants to independent variables at least 5:1; and the independent variables did not meet the conditions of singularity or collinearity. 4. Results There were no significant differences between variables based on gender, except for Ay range (t19 = 3.12, p = .006) and Dpeak torque (t19 = 2.14, p = .046). As such, correlations involving these variables were also considered based on gender. Table 2 shows the correlations between the variables. Significant positive correlations were found between sway area, and Ax range, Ay range and Dpeak torque; Ax range, and Ay range and Dpeak torque; Ay range and Dpeak torque; and, Dpeak torque and Ppeak torque. Significant negative correlations were found between Ppeak torque angle, and sway area, Ax range and Ay range. Significant positive correlations were found amongst male subjects between Ay range, and sway area (r = .724, p = .008), Ax range (r = .622, p = .031) and JPS AE (r = .667, p = .018). Significant positive

Table 2 Correlations between measured variables. Sway area

Ax range

Ay range

AROM

JPS AE

.903** .000

.764** .000

.554** .009

.167 .471

.287 .207

.538* .012

.001 .998

.033 .888

.567** .007

.449* .041

.074 .749

.288 .206

.590** .005

.036 .878

.037 .872

.471* .031

.079 .732

.168 .467

.439* .046

.089 .702

.162 .484

1.000

.112 .630

.442* .045

.314 .165

.255 .264

.008 .972

.079 .732

.112 .630

1.000

.060 .796

.177 .442

.269 .239

.029 .900

.288 .206

.168 .467

.442* .045

.060 .796

1.000

.213 .353

.075 .746

.077 .741

.538* .012

.590** .005

.439* .046

.314 .165

.177 .442

.213 .353

1.000

.260 .256

.065 .781

Pearson correlation Sig. (2-tailed)

.001 .998

.036 .878

.089 .702

.255 .264

.269 .239

.075 .746

.260 .256

1.000

.058 .804

Pearson correlation Sig. (2-tailed)

.033 .888

.037 .872

.162 .484

.008 .972

.029 .900

.077 .741

.065 .781

.058 .804

1.000

Sway area

Pearson correlation Sig. (2-tailed)

Ax range

Pearson correlation Sig. (2-tailed)

.903** .000

Ay range

Pearson correlation Sig. (2-tailed)

.764** .000

.567** .007

Dpeak torque

Pearson correlation Sig. (2-tailed)

.554** .009

.449* .041

.471* .031

Dpeak torque angle

Pearson Correlation Sig. (2-tailed)

.167 .471

.074 .749

Ppeak torque

Pearson correlation Sig. (2-tailed)

.287 .207

Ppeak torque angle

Pearson correlation Sig. (2-tailed)

AROM

JPS AE

1.000

1.000

1.000

Dpeak torque

Dpeak torque angle

AROM, active range of motion; JPS AE, joint position sense absolute error; Sig., significance value. * p < .05. ** p < .01.

Ppeak torque

Ppeak torque angle

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correlations were found amongst female subjects between Ay range and sway area (r = .709, p = .032). Regression analyses for the independent variables significantly correlated with each dependent variable show that PPeak torque angle and Dpeak torque significantly predict 45.4%, 42.5% and 31.6% of the variance associated with sway area, Ax range and Ay range, respectively (R2 = 454, F = 7.482, p = 004; R2 = 425, F = 6.658, p = 007; R2 = .316, F = 4.149, p = 033). Significant standard regression coefficients were noted for Ppeak torque angle and Dpeak torque when considering sway area (b = .404, t = 2.202, p = .041; b = .427, t = 2.326, p = .032); and Ppeak torque angle when considering Ax range (b = .498, t = 2.648, p = .016). All tolerance levels were high, showing that singularity and multi-collinearity assumptions were not met.

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There was no significant association between sagittal plane ankle proprioception and control of balance in unilateral stance found in this investigation amongst young, adult athletes, which concurs with the findings in young, adult dancers [23]. Neither was there any significant association between dorsiflexion AROM and control of balance in unilateral stance amongst young, adult athletes. When comparing the findings for ROM association to previous literature, in the adult population (25.9  6.7 years), passive dorsiflexion ROM has been found to significantly correlate (r = .53, p < 0.01) to the anterior direction of the star-excursion balance test (SEBT) but not with the other five directions [24]. Whereas, dorsiflexion AROM in young (21.0  0.3 years) subjects, was not a predictor of unilateral stance control [25]. 5.2. Implications of the findings

5. Discussion 5.1. Analysis of results The data shows that plantarflexion stiffness, in the form of normalised PR, is significantly associated with better control of balance in unilateral stance amongst athletic adults (r = 0.439 to 0.590) This association infers that as a subject sways posteriorly, intrinsic PR during plantarflexion, potentially from tibialis anterior muscle stiffness, may act to maintain stabilisation. Whereas maximal PR in dorsiflexion is significantly associated with poor control of balance in unilateral stance amongst healthy adults (r = .449–.554). These two factors can predict 31.6–45.4% of the variance associated with the various measures of balance control. When considering previous literature, plantarflexion stiffness has received little attention, with most investigations focussing on dorsiflexion characteristics and the associated gastrocnemius muscle. Onambele et al. did identify that relative EMG activity was greater in the tibialis anterior compared with the gastrocnemius in both elderly and young adults during eyes-closed condition (520% c.f. 275%; 191% c.f. 168%) and elderly adults during eyes open condition (193% c.f. 169%) [21]. Whereas, during the eyes open condition for the younger adults (the same as this investigation) relative EMG was actually lower in tibialis anterior compared with gastrocnemius (142% c.f. 160%) [21]. However, EMG activity suggests an active control at the joint as opposed to the PR measured in this investigation. So perhaps, a lower absolute EMG activity would suggest a greater, innate PR within the muscle or joint during a certain degree of freedom. As mentioned, dorsiflexion stiffness has received much of the focus, in particular, stiffness at the gastrocnemius tendon. Gastrocnemius tendon stiffness significantly predicted 13.3%, 7.6% and 7.4% of the variance associated with trial duration of an eyes-open unilateral stance condition; Ax normalised to trial duration of an eyes-open unilateral stance condition; and Ax normalised to trial duration of an eyes-closed unilateral stance condition, respectively [21]. Wang identified that older adults (67.1  2.5 years) had significantly lower ground reaction forces (normalised by body weight) upon landing from a maximal counter movement jump compared with younger adults (18.0  0.3 years; 1.02 c.f. 1.2, p < .05) [22]. However, there were no such differences between the two groups identified between dorsiflexion angular stiffness during the landing (0.5 c.f. 0.5 Nm/kg/8) which suggests that as the balance task gets more difficult, the role of ankle stiffness becomes less apparent, especially considering that there was significantly greater knee angular stiffness in the elderly group during landing (0.01 c.f. 0.02 Nm/kg/8, p < .05) [22]. The finding in this investigation that ankle stiffness in dorsiflexion positively correlated with larger sway measures, may be in response to less stiff joints elsewhere in the kinetic chain that perhaps have greater control over balance during unilateral stance.

Initially, it seems that the physiological aspects normally associated with maintaining quiet stance are not prevalent when controlling unilateral stance. However, this investigation was undertaken in healthy, athletic adults, so it may suggest that the associations found amongst elderly subjects, seen in previous literature [21] are prevalent due to an age-specific condition. The lack of a link between certain ankle characteristics and balance control also matches somewhat to unilateral stance comparisons between healthy adults and adults with FAI. Ross and Guskiewicz found no significant difference in measures of Ax range or Ay range between healthy adults and those with FAI [26]. An alternate explanation could be that the hip joint predominates during unilateral stance, as has been suggested in the form of the ‘‘hip strategy’’ [10]. A large amount of literature has indirectly investigated the proposed influence of the hip on unilateral balance, through fatiguing protocols. Hip fatigue has often been shown to have a greater effect than ankle fatigue on the various parameters of unilateral stance balance control in multiple planes and during varying visual conditions [27], which alludes to the fact that the hip may predominate in more challenging stance conditions than quiet stance. Strength training programmes that have focussed on the hip joint have shown varying influences on balance control. Significant improvements in dynamic rather than static balance control were found in middle-aged and older females who undertook a 21-week progressive resistance training programme, which focussed on the hip joint musculature [28]. Granacher et al. administered an 8-week ballistic training programme to the hip, knee and ankle joint musculature to young adults and found significant improvements in COP displacement and both Ax and Ay oscillations during 30 s of unilateral stance. However, these improvements were not significantly greater than the improvements seen in a control group after 8 weeks without training [29]. As yet, no literature has focussed on developing physiological characteristics (such as stiffness, proprioception and flexibility) purely in the hip and the subsequent effects on balance performance. With further understanding of the proposed physiological factors that influence the control of challenging balance conditions, more effective training regimens could be implemented in the athletic community to enhance performance and minimise injury risk. The limitations to the study in terms of methodology were associated with the test–retest reliability values of the unilateral stance and JPS tests found during a pilot study. The ICC(2,3) of the scores for the unilateral stance test were similar to those in the literature [15,25], however, the ICC(2,3) for the JPS test suggests that an alternative method could have been used, for instance, using a computer-controlled torque motor [30]. However, this particular piece of equipment was not available to the investigators. When measuring peak torque, the weight of the manipulandum and foot

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was included each time, which may have had an influence on correlation given some variance amongst foot anthropometry within young athletes. Balance is a vital component of physical function both in day to day life and within the athletic realm and the ability to maintain control of unilateral stance is important for the prevention of injuries and optimising performance. This study will have hopefully highlighted that the ankle has limited influence on this, and that further research is required in order to ascertain what are the key factors involved in enhancing this particular aspect of essential human function. Acknowledgements Philip Graham-Smith, for assistance with data analysis, Stephen Horton, for assistance with data collection, Laura Smith, for assistance with data collection. Conflict of interest statement The authors hereby confirm that there are no conflicts of interest associated with this piece of work. References [1] Pollock A, Durward B, Rowe P. What is balance? Clin Rehabil 2000;14(4):402– 6. [2] Maki B, McIlroy W. The role of limb movements in maintaining upright stance: the ‘change-in-support’ strategy. Phys Ther 1997;77(5):488–507. [3] Trojian T, McKeag D. Single leg balance test to identify risk of ankle sprains. Br J Sports Med 2006;40(7):610–3. [4] Wikstrom E, Tillman M, Chmielewski T, Canraugh J, Borsa P. Dynamic postural stability deficits in subjects with self-reported ankle instability. Med Sci Sports Exerc 2007;39(3):397–402. [5] Riemann B, Myers J, Lephart S. Comparison of the ankle: knee, hip, and trunk corrective action shown during single-leg stance on firm, foam, and multiaxial surfaces. Arch Phys Med Rehabil 2003;84(1):90–5. [6] Nashner L, McCollum G. The organization of human postural movements: a formal basis and experimental synthesis. Behav Brain Sci 1985;8(1):135–72. [7] Gatev P, Thomas S, Thomas K, Hallett M. Feedforward ankle strategy of balance during quiet stance in adults. J Physiol 1999;514(3):915–28. [8] Winter D. Human balance and posture control during standing and walking. Gait Posture 1995;3(4):193–214. [9] Cote K, Brunet M, Gansneder B. Effects of pronated and supinated foot postures on static and dynamic postural stability. J Athl Train 2005;40(1):41–6. [10] Horak F, Nashner L. Central programming of postural movements: adaptation to altered support surface conurations. J Neurophysiol 1986;55(6):1369–81.

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