Strategies for equilibrium maintenance during single ... - Gait & Posture

Gait & Posture 44 (2016) 149–154

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Strategies for equilibrium maintenance during single leg standing on a wobble board Priscila de Brito Silva a, Anderson Souza Oliveira a,b, Natalie Mrachacz-Kersting a, Uffe Laessoe a,c, Uwe Gustav Kersting a,* a

Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Fredrik Bajers Vej 7 D-3, 9220 Aalborg, Denmark1 Department of Mechanical and Manufacturing Engineering, Aalborg University, Fibigerstraede 16, Aalborg East 9220, Denmark c Physiotherapy Department, University College North Denmark, Selma Lagerløfs Vej 2 - 9220 Aalborg, Denmark2

b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 19 September 2014 Received in revised form 19 November 2015 Accepted 3 December 2015

The aim of this study was to identify and compare movement strategies used to maintain balance while single leg standing on either a firm surface (FS) or on a wobble board (WB). In 17 healthy men, retroreflective markers were positioned on the xiphoid process and nondominant lateral malleolus to calculate trunk and contralateral-leg excursion (EXC) and velocity (VEL), and center of pressure (CoP) EXC and VEL during FS on a force platform. From the WB test, standing time (WBTIME) was determined and the board’s angular EXC and VEL were calculated from four markers on the WB as surrogate measures for CoP dynamics. Electromyographic average rectified values (ARV) from eight leg and thigh muscles of the supporting limb were calculated for both tasks. WB ARV amplitudes were normalized with respect to the value of FS ARV and presented significantly higher peroneus longus and biceps femoris activity (p < 0.05). WB standing time was correlated to trunk sagittal plane velocity (r = 0.73 at p = 0.016) and excursion (r = 0.67 at p = 0.03). CoP and WB angular movement measures were weakly and not significantly correlated between tasks. This lack of correlation indicates that WB balance maintenance requires movement beyond the ankle strategy as described for the FS task. WB standing likely demands different biomechanical and neuromuscular control strategies, which has immediate implications for the significance of WB tests in contrast to FS balance tests. Differences in control strategies will also have implications for the understanding of mechanisms for rehabilitation training using such devices. ß 2015 Published by Elsevier B.V.

Keywords: Balance Balance board Ankle disc Motor control Injury prevention

1. Introduction Altering the support surface is a widely used technique to challenge balance control during standing as a means of training of postural stability [1–4]. Wobble boards (WB, also called balance boards or ankle discs) have been used as part of neuromuscular training programs to enhance proprioception and balance control, especially among young adults and teenagers [5]. Training programs including such devices are effective in improving leg muscle reaction time and burst duration when experiencing

* Corresponding author. Tel.: +45 99408094; fax: +45 98154008. E-mail addresses: [email protected] (P.d.B. Silva), [email protected] (A.S. Oliveira), [email protected] (N. Mrachacz-Kersting), ufl@ucn.dk (U. Laessoe), [email protected] (U.G. Kersting). 1 Tel.: +45 9940 8827. 2 Tel.: +45 7269 5000. http://dx.doi.org/10.1016/j.gaitpost.2015.12.005 0966-6362/ß 2015 Published by Elsevier B.V.

perturbations to balance in young adults [1,6], as well as in improving balance in both static and dynamic conditions in stroke patients [2] and elderly people [3]. Training programs including such devices have been shown to be effective in improving leg muscle reaction time and burst duration when experiencing perturbations to balance in young adults [1,6] as well as in improving balance in both static and dynamic conditions in stroke patients [2] and elderly people [3]. Multimodal neuromuscular training programs, including WB training, reduce lower limb injury incidences when there is no ankle instability [4,7,8] and improve risk factors for sustaining an ankle sprain [9,10]. To date, little is known regarding the required strategies to maintain equilibrium when standing on a WB, i.e., how the coordination of segmental movements and muscle activity is used to control the center of mass (CoM) position and the movement of the board. Depending on the stability of the support surface, different sensory-motor strategies are likely required in order to

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control the CoM [11]. In an attempt to establish levels of stability, previous investigations have reported either the amount of time subjects were able to stand on unstable devices [9,12] or postural stability indices from various types of commercially available equipment that use unstable support surfaces [6,13,14]. These previous studies provided simple and useful approaches for describing performance, however, a more focused analysis on how balance maintenance is achieved during WB exercises was not explored. Hof [15] has theoretically derived three different mechanisms which allow for balance maintenance during standing tasks. The first mechanism is to move the center of pressure within the base of support which is described by the inverted pendulum model. The second mechanism dictates that if the base of support is small, or too small, for the first mechanism to prevent a loss of balance a counter-rotation mechanism can be employed which extends the area in which balance can be regained by up to 6 cm beyond the base of support [10,14]. This counter-rotation mechanism is achieved by movements of free segments around the center of mass, i.e., arms, upper trunk and/or the free leg. The third mechanism named was to apply an external force by leaning to something or grabbing a rail which is not relevant in this context. As the base of support is theoretically just one point during WB standing it is likely that mainly the second mechanism is used. However, no experimental data exist, to the best of the authors’ knowledge, on standing on a WB or comparison to single leg standing on a firm surface (FS). This is surprising since single leg standing tests on a firm surface have been widely used to investigate postural stability and balance control [2,3] also following WB training. Here, the variability and/or velocity of the center of pressure (CoP) displacement during single leg standing have been directly related to ankle instability [16–18] and indirectly to ankle injury risk [19]. If standing on a wobble board does indeed require different mechanisms of balance maintenance it is likely that parameters derived from a WB standing test provide additional insights into the relationship of balancing ability during dynamic tasks and injury risk. The aim of this study was to identify how muscle activity and segmental movements control balance when performing single leg standing on a FS as opposed to WB. Specifically, we were interested in the trunk segment and the contralateral leg to identify to which extent segmental rotations are required to maintain balance. We hypothesized that balance measures obtained from FS and WB tests are not related and, second, that the strategies to maintain balance in either condition differ.

2. Methods 2.1. Subjects Seventeen healthy men volunteered for the experiment (age: 28 4 yrs; body mass: 69 8 kg; body height: 173 5 cm). All subjects were right-leg-dominant as determined by a kicking test [19] and the dominant limb was used for testing. The participants in this study were recreational practitioners of different team sports (soccer, basketball, handball, ice hockey). Participants reported to partake in physical activities about 3–4 times per week. Exclusion criteria included a history of knee or ankle ligament or other joint injury, current lower-extremity injury, recent (within the last 6 months) low back injury, or vestibular dysfunction. In addition, previous experience and/or systematic training using the wobble board would lead to exclusion. All subjects provided written informed consent before participation and the procedures were approved by the ethical committee of North Jutland (N-20100042).

2.2. Experimental setup Postural stability was measured during one evaluation session. Initially, familiarization procedures were performed and included explanation of both tasks, while allowing the subjects to practice assuming the test position. For the WB test the familiarization period was 1 min. Subsequently, the preparation of the subjects involved placement of spherical retroreflective markers for kinematic analysis and electrodes for electromyographic (EMG) recordings. Subjects were then asked to perform 3 15 s single-leg standing on a force platform without the wobble board. They were instructed to stay as still as possible with the hands akimbo, while keeping the contralateral hip and knee slightly flexed with the foot at least 10 cm above the floor. After a 3-min rest period, subjects were asked to perform one single-leg standing trial on the WB (34 cm diameter wooden board with rubber surface, with a half wooden sphere with 6 cm height and 13 cm diameter as base of support – maximal tilt angle = 308), which was placed on a force platform (Fig. 1A), described at session below. Subjects were instructed to start with hands akimbo and attempt to keep the board flat (08 tilt) and as still as possible for as long as possible within a 60-s recording period, maintaining the contralateral limb away from the ground and the board. In order to fulfill this premise, offline visual inspection of motion capture recordings was used to identify the longest period in which each subject successfully maintained his balance on the WB–WB standing balance duration (WBTIME). Across all participants times ranged from 7.0 to 41.9 s. 2.3. Kinetics A three-dimensional force platform (AMTI, OR6-5, Watertown, MA) provided ground reaction forces and moments sampled at 2048 Hz, simultaneously with marker data by a motion capture system (eight cameras, Oqus 300, Qualisys, Gothenburg, Sweden) at 256 Hz. Signals were digitally low-pass filtered with a 4th order zero-lag Butterworth filter (50 Hz). The excursion of the center of pressure (CoPEXC) as well as the average velocity of the center of pressure (CoPVEL) displacement in the sagittal and frontal planes were calculated for the last 10 s of FS. 2.4. Kinematics Retroreflective spherical markers were placed on the lower endpoint of the sternum (xiphoid process), lateral malleolus of the left (contralateral) lower limb, as well as on four equidistant positions on the WB (Fig. 1A), in order to define the displacement of the device, the trunk and contralateral leg. Marker positions were tracked using a commercial tracking software (QTM 2.9 Qualisys, Gothenburg, Sweden). Offline analyses were performed after filtering marker positions (10 Hz, 4th order low-pass, zero-lag Butterworth filter). The total excursion and average velocity of the trunk and contra-lateral leg markers (TKVEL and CLVEL, respectively) were calculated in the sagittal and frontal planes for both FS and WB tests. 2.5. Wobble board analysis The movement of the WB was chosen as a surrogate measure to match the parameters extracted from the CoP movement and was based on the markers positioned on the board (Fig. 1A). These markers were used to calculate the average of the resultant WB angular amplitude (WBANG) and angular velocity (WBVEL), in both planes. The excursion of the WB angular displacement (WBEXC) was calculated as the sum of WB angle variances in both planes for the whole WB standing time duration as has been described for CoP excursion [20].


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Fig. 1. (A) Illustration of the single-leg standing on a wobble board experimental setup performed on a force platform, representing a 5-s balance period (light gray area within dotted black lines) obtained from WB displacement for sagittal plane (SP – in black) and frontal plane (FP in gray) directions (plot). In B, data from the 5-s balance period. In C, surface electromyography corresponding to the balance period for eight muscles from the supporting limb are presented.

To investigate the movement strategies used to maintain balance, a stable period was defined for each subject. The data corresponding to the first 7-s period of maintained balance were selected for each subject (dark gray shaded area – Fig. 1A). To exclude any body actions related to finding a stable position after touching the ground or before touching it when loosing balance only the middle 5 s of the stable period were used for analysis. This procedure was arbitrarily chosen to ensure a 5-s period representing the balance period for all subjects (light gray shaded area within segmented lines – Fig. 1A).

2.6. Electromyography Surface EMG signals were recorded in a bipolar configuration with pairs of Ag/AgCl electrodes (Ambu Neuroline 720 01-K/12; Ambu, Ballerup, Denmark) and 22 mm of center-to-center spacing. The EMG signals were amplified with a gain of 2000 (EMG-USB, LISiN; OT Bioelettronica, Turin, Italy), A/D converted (12 bit), sampled at 2048 Hz. A reference electrode was placed at the right wrist. The EMG signals of the right limb were recorded from tibialis anterior (TA), peroneus longus (PL), soleus (SOL) gastrocnemius


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medialis (GM), rectus femoris (RF), vastus lateralis (VL), semitendinosus (ST) and biceps femoris (BF) according to SENIAM [20]. An external trigger synchronized EMG, ground reaction force and kinematic data collection. EMG signals were digitally filtered (2nd order, zero-phase-lag Butterworth filter, 20–500 Hz) and fullwave rectified. Average rectified values (ARV) were calculated in moving windows of 500 ms with a 250 ms progression along the period of analysis of each test. The average ARV obtained from these moving windows was used for analysis. Wobble board ARV results were expressed as a percentage of the respective muscles obtained during standing on the FS.

nor the contralateral leg velocity presented significant differences between planes (Table 2). The average CoP and trunk velocities, however, were significantly larger in the frontal plane as compared to the sagittal plane (49.5% and 22.2% at p = 0.007 and p = 0.003, respectively). For standing on the WB, neither angular excursion of the board nor trunk or contralateral leg velocity differed between planes. On the other hand, the tilting velocity of the WB was larger in the frontal plane (24.9%, p = 0.009). The relation between movement ranges in both planes was inverse for each task, with a higher range in the frontal plane for CoP and higher angular amplitude for WB on the sagittal plane (FP/SP ratio of 0.7 and 2.0, respectively).

2.7. Statistical analysis 3.2. Lower limb muscle activity Based on the fixed time-windows as they were defined in the section ‘kinetics’, the Wilcoxon signed-rank test was used to analyze differences between sagittal (SP) and frontal (FP) planes for FS CoPVEL, WBANG WBVEL for WB as well as TKVEL and CLVEL for both tasks. In addition, the Friedman test was applied in order to identify differences among muscle activities obtained from the 5-s stable period, followed by a Wilcoxon signed-rank test for post-hoc comparisons. Spearman’s rho was calculated among variables within each task and also among excursion and velocity of the CoP and the WB as well as WB standing duration to correlate general balance performance between both tasks. The significance level was set to p < 0.05, except for multiple comparisons by the Wilcoxon signedrank test where the significance level was corrected for 28 comparisons (p < 0.0018). During pilot tests, the reliability of WB board data for the 5-s stable period used to analyze balance maintenance was verified. Intra-class correlation coefficients (ICC) were calculated between the dependent variables obtained from the WB test of two tests separated by a 4-week period (n = 10). The ICCs were as follows: 0.84 for average frontal plane WB angular velocity, 0.72 for absolute WB angle, 0.57 for WB average sagittal plane angular velocity and 0.53 for absolute angle amplitude.

3. Results 3.1. General balance performance The CoP excursion could only be determined for the FS condition and was on average 64.6 mm. The trunk excursion was used for both FS and WB to compare performance in these two different tasks. The trunk excursion was 227% when standing on the WB as compared to FS standing. The contralateral leg had on average an over six times larger excursion on the WB (Table 1). The total CoP and WB excursions (Table 1) are provided as surrogate measures but were not statistically compared. Table 1 also contains the average time of the stable period across the tested subjects as a reference. Separating the results for the main anatomical planes (sagittal and frontal) revealed that for FS neither the average CoP amplitude Table 1 Mean (SD) trunk and contralateral leg excursion for one leg standing on a firm surface (FS) and on the wobble board (WB), as well as excursion of center of pressure (CoP), WB angle and standing time (WBTIME).

CoP excursion (mm) Trunk excursion (mm) Contralateral leg excursion (mm) WBEXC (8) WBTIME (s)

During the WB task, all muscles presented activation above 100% of FS muscle activation with significant differences between relative activation amplitudes within the WB task (p = 0.002, Fig. 2). Wilcoxon comparisons revealed that PL activation was significantly higher in comparison to SOL and ST (p < 0.0018), while BF activation was higher when compared to VL, RF and ST (p < 0.0018). No differences were observed between the relative PL and BF activations. 3.3. Correlations Spearman’s rho coefficients of correlation between dependent variables from single-leg standing on the FS, the WB, and between both tasks (FS WB) are summarized in Table 3. For the FS task, contralateral leg velocity in the sagittal plane was moderately correlated with sagittal plane CoP velocity (r = 0.55). Only weak and non-significant correlations were detected between the CoPrelated variables and the parameters describing trunk and contralateral leg kinematics. For the WB task, total trunk excursion was significantly negatively correlated with WB standing time (r = 0.67, p = 0.03) and trunk velocity in the frontal plane (r = 0.73, p = 0.016). Both trunk and contralateral leg excursions were significantly correlated to WB excursion (r = 0.685 at p = 0.029; r = 0.636 at p = 0.048, respectively) and WB excursion velocity in the sagittal plane with total trunk excursion (r = 0.636 at p = 0.048). Only weak and no other significant correlations were found between the descriptors of WB kinematics and the kinematic parameters describing contralateral leg and trunk movement (Table 3). Between both tasks there was no significant correlation between CoP-related variables and the descriptors of WB kinematics.

Table 2 Mean (SD) of sagittal (SP) and frontal planes (FP) average velocity for CoP, trunk and contralateral leg during one leg standing on a firm surface (FS), WB angular velocity, trunk, contralateral leg velocity during single-leg standing on WB. Firm surface

SP

FP

CoP displacement (mm) CoP velocity (mm s 1) Trunk velocity (mm s 1) Contralateral leg velocity (mm s

18.0 10.1 3.3 1.1 0.64 0.13 1.2 0.4

20.6 15.1 5.0 1.6* 0.77 0.26* 1.4 0.7

1

)

FS

WB

Wobble board

SP

FP

64.6 18.3 12.0 2.6 25.8 10.2 – –

– 27.4 8.9 155.9 136.8 161.3 59.5 24.4 10.3

WB angle (8) WB velocity (8 s 1) Trunk velocity (mm s 1) Contralateral leg velocity (mm s

5.0 3.7 18.1 6.7 4.0 1.5 23.9 23.2

4.8 1.9 22.6 9.1* 3.6 1.4 25.0 20.2

*

1

)

Denotes a significant difference for the sagittal plane (p < 0.05).


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Muscle activation during WB 600

*

**

ARV (% FS)

500 400 300 200 100 0

PL

TA

SOL

GM

VL

RF

ST

BF

Muscles Fig. 2. Mean (SD) normalized averaged rectified values (ARV) of the electromyographic activity (EMG) recorded from dominant lower limb muscles during 5-s balance period of wobble board test. Muscle nomenclature is detailed in Section 2. * denotes significant difference in relation to SOL and ST (p < 0.0018). ** denotes significant difference in relation to VL, RF and ST (p < 0.0018).

4. Discussion The purpose of this study was to identify and compare balance maintenance strategies when performing single leg standing on a FS and on a WB. Results revealed that standing on a WB requires substantially greater trunk and contralateral leg movements while muscle activity was increased for selected leg muscles but also one hip extensor muscle. There were only weak to no correlations between parameters describing balancing performance in both conditions. This suggests that different strategies are used to solve the respective tasks, such that these may not be considered synonymous when testing subjects’ balance performance. This has implications not only for the assessment of balance following injury and within a rehabilitation process, but also for their potential value in predicting injury risk. The present investigation obtained CoP displacement values similar to previous studies [7,20] on healthy subjects performing single leg standing on a firm surface. On the other hand, there were no papers identified which would allow for a comparison of the defined surrogate measures for WB movement. The findings of this study comply with Riemann et al. [21] as the control of standing balance during a single leg standing task relies on the control of the

Table 3 Spearman’s rho coefficients of correlation between dependent variables from single-leg standing on the wobble board (WB), firm surface (FS) and between both tasks (FS WB) test. WB time represents the duration of standing time (s), WB/CoP represents the amplitude variable for WB angle measured during WB test, CoP (center of pressure) obtained during FS test, trunk (TK) and contralateral leg (CL) displacement; VEL – velocity; SP – sagittal plane; FP – frontal plane; EXC – excursion. Significant correlations are highlighted by an asterisk and bold font. FS CoPVEL SP CoPVEL FP CoPEXC WB WB Time WBEXC WBVEL SP WBVEL FP FS WB

TKVEL SP

TKVEL FP

CLVEL SP

CLVEL FP

0.23 0.08 0.02

0.14 0.08 0.06

0.55 0.16 0.09

0.40 0.21 0.12

TKVEL SP

TKVEL FP

CLVEL SP

CLVEL FP

0.39 0.53 0.61 0.30

0.73* 0.56 0.48 0.44

0.56 0.52 0.56 0.36

0.62 0.59 0.49 0.43

WB time

WBEXC

0.01 0.018 0.01

0.00 0.30 0.07

CoPEXC CoPVEL SP CoPVEL FP *

Indicates p < 0.05.

WBVEL SP 0.03 0.27 0.07

TKEXC

CLEXC

0.25 0.32 0.39

0.35 0.00 0.12

TKEXC 0.67* 0.68* 0.64* 0.49

CLEXC 0.61 0.64* 0.58 0.50 WBVEL FP 0.06 0.20 0.14

ankle with increasing contributions of proximal joints as the balance demands become more challenging [21] such as single leg standing on a WB as assessed in the current study. There are different movement strategies used to return the body to equilibrium in a stance position. While it has been described that the ankle control strategy results in only small amounts of body sway when standing on a firm surface [21,22], strategies to maintain equilibrium while standing on less stable surfaces may rely either on plantar flexor or hip extensor muscles, or a combination thereof to control CoM accelerations [22], depending on the support offered [11]. Moreover, a theoretical base has been provided for a mechanism using counter rotations of segments with respect to the CoM to enhance the limits of stability [15]. The rounded surface of the WB used in the present study was effective in providing high levels of instability and, therefore, eliciting reactive strategies especially from the contralateral leg. This observation corroborates with the negative correlation identified between frontal plane trunk velocity and WB standing time duration, showing that the better trunk velocity was controlled by the subject the longer subjects could stand on the WB. The PL muscle had a significantly higher activation in comparison to FS standing, likely to maintain the board flat and still and this was accompanied by segmental rotations required to immediately counteract the acceleration of body segments in an attempt to restore equilibrium. It has been implicated that in order to achieve equilibrium maintenance while performing the WB test, the control of the CoM combined with stabilizing the support surface is required [23]. A similar strategy was revealed in the present study regarding WB control, in which greater PL activity was interpreted as a primary mechanism to stabilize the WB position. At the same time, higher BF activity may reflect an attempt to control accelerations of the trunk segment. The mean activations of TA, GM and SOL were elevated but no significance was shown. This may be due to inter-subject variability in using these muscles but also to the low p-value due to multiple pairwise comparisons. Studies on risk factors for ankle injuries [17] as well as studies using WB devices for preventative or rehabilitative training [24,25] discuss that strength of ankle muscles and, related to that, ankle stiffness are important. It has been implicated that WB and other proprioceptive training enhances muscular strength at the ankle joint. While it is not deniable that the effects of wobble board training are multifactorial [17] the present results indicate that hip muscles and non-support segmental movements are to a much larger extent required on a WB as compared to FS. Therefore,

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including free leg and upper extremity movements in the analysis of injury prone situations when, for example, unexpected perturbations occur [26], may advance the understanding of the benefits of WB exercises to enhance postural responses. Further, to confirm the clinical value of both test paradigms, future research should aim at comparing their respective predictive value in longterm intervention studies. Supraspinal pathways have previously been shown to affect postural responses during balance maintenance [27,28]. These were demonstrated by increased corticospinal excitability and EEG-EMG coherence and increased muscular cortical representation areas [29]. Stance stability following balance training was well correlated to reduced cortical, but not spinal excitability, suggesting that relevant neural adaptations to balance training are achieved at the supraspinal level. Therefore, it may be likely that adaptations to WB training include a coupled adaptation of mechanical control mechanisms and neurological adaptations beyond a simple elevation of muscle activity around the joint of interest. Further research on specific training interventions is needed in order to better understand the coupling of mechanical and neurophysiologic mechanisms for adaptation to balance training. Continuing this track of thought, it has been suggested that the more demanding the task the more sensitive it will be for identifying neuromuscular dysfunctions [9,23], effects of training [14,30] or fatigue impairments [31]. Single leg standing tests may not be challenging enough for identifying impairments to balance and/or postural control in healthy subjects with no history of ankle sprains nor ankle instability, which may be relevant for preventing sports injuries [30]. Dynamic tasks that require complex dynamic control of the CoM, increased sensory weighting to vestibular and visual information [32] may be more relevant in this group of people, as it occurs during sports practice. 5. Conclusion This study demonstrates that equilibrium maintenance on the WB requires responses beyond the ankle strategy mainly used during the FS task performance. Therefore, the evaluation of balance performance can be further explored by means of a WB when higher demands of postural control are induced. Future research may consider this methodology to evaluate balance maintenance, providing an identification of postural control deficits that are crucial to protect from injury. Conflict of interest All authors of this paper declare that they have no conflict of interest. References [1] Oliveira AS, Brito PS, Farina D, Kersting UG. Unilateral balance training enhances neuromuscular reactions to perturbations in the trained and contralateral limb. Gait Posture 2013;38:894–9. [2] Onigbinde AT, Awotidebe T, Awosika H. Effect of 6 weeks wobble board exercises on static and dynamic balance of stroke survivors. Technol Health Care 2009;17:387–92. [3] Ogaya S, Ikezoe T, Soda N, Ichihashi N. Effects of balance training using wobble boards in the elderly. J Strength Cond Res 2011;25:2616–22. [4] Verhagen E, van der Beek A, Twisk J, Bouter L, Bahr R, van Mechelen W. The effect of a proprioceptive balance board training program for the prevention of ankle sprains: a prospective controlled trial. Am J Sports Med 2004;32:1385–93.

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