Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot

Physical Therapy in Sport xxx (2018) 1e8

Contents lists available at ScienceDirect

Physical Therapy in Sport journal homepage: www.elsevier.com/ptsp

Original Research

Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot Martin Alfuth a, *, Markus Gomoll b a b

Niederrhein University of Applied Sciences, Faculty of Health Care, Therapeutic Sciences, Reinarzstr. 49, 47805 Krefeld, Germany German Sport University Cologne, Department of Further Education, Am Sportpark Müngersdorf 6, 50933 Cologne, Germany

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 April 2017 Received in revised form 20 December 2017 Accepted 6 January 2018

Purpose: To investigate the activity of lower extremity muscles in response to single-leg stance on a training device, destabilizing the forefoot while the rearfoot stands on a fixed plate and vice versa compared with a balance pad and the floor. Design: Cross-sectional study. Setting: University's laboratory. Participants: Twenty-seven healthy adults. Methods: Surface electromyography and 2D video analysis were used to record the activity of lower extremity muscles and to control sagittal knee joint angle during single-leg stance trials under one stable control condition and five unstable conditions. Results: The majority of lower extremity muscles were significantly more active when the forefoot was destabilized while the rearfoot remained stable compared with the stable condition and the conditions where the forefoot was stable and the rearfoot unstable (p <0 .001). Mean change of knee joint angle was significantly increased under the conditions rearfoot stable/forefoot unstable (p ¼ 0.001). The soleus muscle activation was significantly increased when balancing on the balance pad (p < 0.001). Conclusions: Increased activity in the majority of lower extremity muscles and sagittal knee joint angles indicate that destabilizing the forefoot while the rearfoot remains stable is the most challenging balance task. Soleus muscle activation increased when performing ankle plantarflexion on the soft balance pad. © 2018 Elsevier Ltd. All rights reserved.

Keywords: Balance task Muscle activation Forefoot Destabilization

1. Introduction Sensorimotor/balance exercises are commonly used for the treatment of chronic ankle instability (Eils & Rosenbaum, 2001; Sefton, Yarar, Hicks-Little, Berry, & Cordova, 2011) or other sports-related injuries that are associated with impaired proprioception and neuromuscular control (Culvenor et al., 2016; Hatton et al., 2016). They aim at decreasing sensorimotor deficits (Freeman, 1965) and restore neuromuscular activation that allows for active joint stability (Wolburg, Rapp, Rieger, & Horstmann, 2016). Balance exercises are usually performed in double- or single-leg stance on devices with different stability properties. Single-leg stance is used for training and testing because poor balance during single-leg stance might predict an increased risk of ankle sprain (McGuine, Greene, Best, & Leverson, 2000; McKeon &

* Corresponding author. E-mail address: [email protected] (M. Alfuth).

Hertel, 2008; Trojian & McKeag, 2006). During these tasks within a long time interval, feedback from joint mechanoreceptors can be usually used by the sensorimotor subsystems, indicating that closed-loop control mechanisms are involved to control the ankle and foot joint movements (Collins & De Luca, 1993; Gutierrez, Kaminski, & Douex, 2009; Mitchell, Collins, De Luca, Burrows, & Lipsitz, 1995). Several therapy devices, such as balance boards and pads, soft mats, air cushions or tilting platforms (De Ridder, Willems, Vanrenterghem, & Roosen, 2015; Pfusterschmied et al., 2013; Verhagen et al., 2004) are incorporated into balance exercises. These devices might primarily address stabilization of ankle motion coupled to talocrural and subtalar articulations. According to Freeman (Freeman, 1965) a sprained ankle generates a varus instability of the talus in the ankle mortise, probably resulting in chronic subtalar instability (Pisani, Pisani, & Parino, 2005). Numerous patients reported a feeling of instability without showing clinical or radiological abnormality (Freeman, 1965), however, subtalar instability is often caused by damage of the

https://doi.org/10.1016/j.ptsp.2018.01.002 1466-853X/© 2018 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Alfuth, M., & Gomoll, M., Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot, Physical Therapy in Sport (2018), https://doi.org/10.1016/j.ptsp.2018.01.002

2

M. Alfuth, M. Gomoll / Physical Therapy in Sport xxx (2018) 1e8

calcaneofibular and interosseous ligaments creating increased rearfoot inversion (Choisne, Hoch, Bawab, Alexander, & Ringleb, 2013; Hintermann, 1996). Therefore, it is central to consider rearfoot biomechanics in the treatment of ankle instability (Hintermann, 1996). Ankle sprains predominantly occur during sudden unexpected ankle supination (Podzielny & Hennig, 1997), where the sensorimotor subsystems mainly operate without feedback (open-loop control mechanisms) to control the ankle-foot complex (Collins & De Luca, 1993; Mitchell et al., 1995). Morey-Klapsing et al. (Morey-Klapsing, Arampatzis, & Bruggemann, 2005) found that ankle and foot kinematics consistently differ during sudden medial and lateral ankle tilts in single-leg stance and concluded that it is not sufficient to only focus on one joint to understand the behavior of the ankle-foot complex. The human ankle-foot complex includes six independent functional segments (De Mits et al., 2012), more than 30 articulations, allowing mostly for 6 degrees of freedom of movement (Morrison & Kaminski, 2007). Passive, active and neural subsystems are intertwined to ensure structure and control of the foot (McKeon & Fourchet, 2015; McKeon, Hertel, Bramble, & Davis, 2015). Pronated and supinated foot types (Cote, Brunet, Gansneder, & Shultz, 2005; Hogan, Powden, & Hoch, 2016; Tsai, Yu, Mercer, & Gross, 2006) as well as cavus, rectus and planus foot types (Hertel, Gay, & Denegar, 2002) might influence postural stability. Injury of the midfoot and forefoot occur frequently and can be a comorbidity in lateral ankle sprain and chronic ankle instability (Fraser, Feger, & Hertel, 2016). Therefore, balance training devices that address the stabilization of the movement between forefoot and rearfoot, occurring in the transverse tarsal joint (calcaneocuboid joint) around two separate axes of rotation (Manter, 1941), during singleleg stance might be of great importance for the prevention and in the rehabilitation of ankle sprains. The muscles of the lower leg contribute to ankle and foot control during single-leg standing (Konradsen, Ravn, & Sorensen, 1993). Muscle activity changes while standing on devices with different properties (Strom et al., 2016; Wolburg et al., 2016). Balance training on different unstable devices is used to restore function of muscles after injury, because during balance exercises muscle activity is increased (Borreani et al., 2014; Braun Ferreira et al., 2011). Increased muscle activity is a worthwhile resource in the sensorimotor recovery of the ankle (Braun Ferreira et al., 2011). Especially the peroneus longus muscle seems to play an important role, because it is the major evertor of the ankle-foot complex and therefore might withstand the inversion moment during the typical injury mechanism (Konradsen, Olesen, & Hansen, 1998). However, it has to be considered that reflex reaction to sudden inversion appears too slow to protect the ankle (Konradsen, Voigt, & Hojsgaard, 1997). Single-leg stance is primarily characterized by an inter-joint coordination, where axial rotation between the ankle and hip joints, and between ankle inversion/eversion and hip axial rotation are crucial (Liu et al., 2012). Knee joint kinematics may differ when balancing on devices with different stability properties (Pfusterschmied et al., 2013). Particularly, the corrective action of the knee joint became increasingly important when a single-leg balance task became more challenging, e.g. from firm to foam surface (Riemann, Myers, & Lephart, 2003). Therefore, the analysis of knee kinematics might be important when single-leg stance with increasing levels of instability is performed. There is a lack of information about how muscles react and sagittal knee kinematics change on a training device (ARTZT vitality® Mini Stability Trainer, Ludwig ARTZT GmbH, Dornburg, Germany) that selectively destabilizes the forefoot while the rearfoot stands on a fixed plate and vice versa. The aims of the study were to investigate activity of lower extremity muscles and sagittal

knee joint kinematics in response to single-leg stance on the Mini Stability Trainer (MST), a) while destabilizing the forefoot with the rearfoot standing on a fixed plate and b) while destabilizing the rearfoot with the forefoot fixed, compared with a common unstable balance pad (BP) and the floor. It was hypothesized that single-leg stance using the MST results in increased activity of selected distal and proximal lower extremity muscles and increased sagittal knee joint range of motion compared with the floor and the BP. 2. Methods 2.1. Participants Twenty-seven healthy participants - 11 female and 16 male volunteered to participate in the study. Participants were recruited from the local university and local sport clubs and selected using a self-constructed questionnaire. None of the participants had a history of a traumatic injury or surgery of the lower extremity, the pelvis, and/or trunk within the past twelve months. No subject reported a chronic ankle instability according to the recommendations of the ‘International Ankle Consortium’ (Gribble et al., 2013) or any other chronic disorder of the lower extremity. Participants were also excluded if they had acute pain, dysfunction or pathological foot deformities. The mean (SD) age, height, body mass, and body mass index of included participants was 25.5 ± 4.2 years, 177.0 ± 10.0 cm, 69.7 ± 10.2 kg, and 22.2 ± 1.8 kg/m2, respectively. An a priori sample size calculation on the basis of a < 0.05 and a moderate effect size of dz ¼ 0.5 from dependent t-tests comparing pilot measurements using mean EMG (mV) of the peroneus longus muscle under different test conditions revealed that a sample size of n ¼ 27 was needed to obtain a test power of >80%. All of the participants provided written informed consent prior to participation. 2.2. Procedures After a 2-min warm-up, participants were asked to perform three single-leg quiet stance trials on the randomly allocated leg under one stable control (floor) and 5 different unstable balance conditions. Therefore, two different unstable devices were used: 1. The MST consists of different plates with different surface structures on the bottom side of the plates (Fig. 1 and Table 1) that can be combined to separately induce instability of the forefoot or the rearfoot in single-leg stance. The green plate has two parallel, peripheral half rolls at the bottom side (Fig. 1, a) and a flat surface at the top side, ensuring a stable stance of the respective part of the foot. The blue plate has a central half roll at the bottom side (Fig. 1, b) and a flat surface at the top side, inducing medial or lateral tilting of the respective part of the foot. The red plate has a central hemisphere at the bottom side (Fig. 1, c) and a flat surface at the top side, inducing multidirectional tilting of the respective part of the foot. 2. The BP (ARTZT vitality® Stability Trainer, Ludwig ARTZT GmbH, Dornburg, Germany) consists of soft material with horizontal grooves at the top side (Fig. 1, d and Table 1) and a flat surface at the bottom side, inducing instability of the ankle in all directions. At first, each participant completed the trials on the floor. The 5 unstable conditions were (Fig. 1 and Table 1):  MST [forefoot stable (a)/rearfoot unstable (b), inducing an excursion of the rearfoot in the frontal plane]

Please cite this article in press as: Alfuth, M., & Gomoll, M., Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot, Physical Therapy in Sport (2018), https://doi.org/10.1016/j.ptsp.2018.01.002

M. Alfuth, M. Gomoll / Physical Therapy in Sport xxx (2018) 1e8

3

Fig. 1. Therapy devices [a ¼ Mini Stability Trainer, stable plate; b ¼ Mini Stability Trainer, unstable plate, frontal plane; c ¼ Mini Stability Trainer, unstable plate, multidirectional (bottom side); d ¼ Balance pad (top side)].

Table 1 Characteristics of the five therapy devices. Balance condition and device

Device or plate combination

Material Dimensions (length x width x height)

Control (stable)

Floor

###

Mini Stability Trainer (forefoot stable/rearfoot unstable in the frontal plane)

Forefoot ¼ a Rearfoot ¼ b

10 cm  10 cm 1 cm 10 cm  10 cm 1 cm 10 cm  10 cm 1 cm 10 cm  10 cm 1 cm 10 cm  10 cm 1 cm 10 cm  10 cm 1 cm 10 cm  10 cm 1 cm 10 cm  10 cm 1 cm 50 cm  40 cm 5.5 cm

Mini Stability Trainer (forefoot stable/rearfoot unstable, multidirectional)

Mini Stability Trainer (rearfoot stable/forefoot unstable in the frontal plane)

Mini Stability Trainer (rearfoot stable/forefoot unstable, multidirectional)

Forefoot ¼ a Rearfoot ¼ c

Rearfoot ¼ a Forefoot ¼ b

Rearfoot ¼ a Forefoot ¼ c

Balance pad (Stability Trainer); black colored, i.e. skill d level: hard

x

Material property

Surface structure (top face)

Surface structure (rear side)

Polyvinylchlorid hard (PVC) plastic hard plastic hard

flat

###

flat flat

Two parallel, peripheral half rolls One central half roll

plastic plastic

hard hard

flat flat

plastic plastic

hard hard

flat flat

Two parallel, peripheral half rolls One central hemisphere Two parallel, peripheral half rolls One central half roll

plastic plastic

hard hard

flat flat

Polyethylene

soft

x x x x x x x x

Two parallel, peripheral half rolls One central hemisphere horizontal grooves flat

 MST [forefoot stable (a)/rearfoot unstable (c), inducing a multidirectional excursion of the rearfoot]  MST [rearfoot stable (a)/forefoot unstable (b), inducing an excursion of the forefoot in the frontal plane]  MST [rearfoot stable (a)/forefoot unstable (c), inducing a multidirectional excursion of the forefoot]  BP Participants were barefoot with their eyes open focusing a target that was 5 m in front of them. The rearfoot was placed centrally on the respective plate of the MST with the posterior border of the calcaneus terminating at the edge of the plate (Fig. 2). The forefoot was positioned centrally on the respective plate, such that the first metatarsal head was placed in the middle of the anterior-posterior diameter with the medial border terminating at the medial edge of the plate. For the BP, the foot was placed centrally on the device. A marker ensured the same placement of the devices on the floor. The knee of the supporting leg was slightly bent and participants' hands were placed on their iliac crest. The order of balance conditions was assigned at random to minimize potential systematic effects of learning. Each trial lasted 20 s with 30-s rest periods between trials. The rest periods between the conditions took about 1 min. The participants were allowed to slightly touch the floor with the top of the great toe of the contralateral foot at most 5 times if necessary, because it turned out during the trials that some of the conditions were very challenging and participants were threatened to fall. A trial was considered as unacceptable and was repeated when the subject left the device, the device was displaced from the usual location during stance, the contralateral foot touched the floor with a larger area than the top

Fig. 2. Participant balancing on the Mini Stability Trainer under the condition forefoot stable and rearfoot unstable multidirectional with reflective markers and electrodes attached to her supporting leg.

Please cite this article in press as: Alfuth, M., & Gomoll, M., Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot, Physical Therapy in Sport (2018), https://doi.org/10.1016/j.ptsp.2018.01.002

4

M. Alfuth, M. Gomoll / Physical Therapy in Sport xxx (2018) 1e8

of the toe or the hands left the usual position more than 3 times. After finishing all balance conditions, participants were asked to simply rank the conditions from most stable to least stable, according to their perceived level of stability. 2.3. Data recording Surface electromyography (EMG) was used to record activity of the tibialis anterior (TA), peroneus longus (PL), soleus (SOL), medial gastrocnemius (GM), long head of the biceps femoris (BF) and vastus medialis (VM) muscles. Bipolar surface electrodes (Noraxon Dual Electrodes) with a 20 mm inter-electrode spacing were applied over the middle portion of the muscle belly parallel to the fiber orientation according to the recommendations of the SENIAM project group (Surface ElectroMyoGraphy for the Non-Invasive Assessment of Muscles; www.seniam.org). Accuracy of electrode placement was verified by palpating the muscle and performing lower limb movements against manual resistance carried out by the assessor. The skin was shaved and cleaned by rubbing with 2propanol prior to electrode application in order to minimize skin impedance (Konrad, 2006). For signal recording a skin impedance 10 kU and an EMG baseline noise level 10 mV in supine resting position were accepted as precondition. EMG signals were recorded using the Desktop DTS EMG System (Noraxon, U.S.A. Inc., Scottsdale, AZ) with a sampling frequency of 1500 Hz. Input impedance of the amplifier was >100 MU (Merletti, Botter, & Barone, 2016). According to the predefined muscles, Noraxon DTS Lossless EMG sensors were secured alongside the respective electrodes (Fig. 2). The sensors that communicate their data with the DTS receiver, were connected to the electrodes using DTS pinch cables. Data were collected and processed using MR 3.9.37 software (Noraxon, U.S.A. Inc., Scottsdale, AZ). All EMG signals were filtered using a 500 Hz low pass filter. They were rectified and smoothed using a root mean square (RMS) algorithm (150 ms). Data from second 5 to second 15 were used for further analysis. For each trial, the mean EMG amplitude over the 10-sec period was calculated, because it is considered the most significant parameter to outline the task specific innervation input of selected muscles and to compare muscle activity patterns (Konrad, 2006). Ensemble averages out of the 3 trials for each condition were computed and used for further evaluation. Individual differences between the 5 unstable conditions and the control condition were determined. Relative effects (median of individual differences along with quartiles in percent) were calculated to normalize data from the unstable conditions to the data from the control condition, that is represented by the dotted zero line (Figs. 3 and 4). Increased knee joint motion seems to be an indicator of corrective action during single-leg balance tasks with augmented instability (Pfusterschmied et al., 2013; Riemann et al., 2003). Therefore, the knee angle ( ) at the beginning of the balance task and the change of knee angle ( ) in sagittal plane were captured using 2D-video analysis (MyoVIDEO Pro - High Speed System, Noraxon, U.S.A. Inc., Scottsdale, AZ) after attaching reflective markers to anatomical landmarks of the participant's supporting leg (Fig. 2). Data were recorded and markers were automatically tracked over the 10-sec. period using the MR 3.9.37 software. The average of the knee angle at the beginning of the balance task was documented. The mean change of the knee angle over the 10-sec. period out of 3 trials was determined for each condition and used for further analysis. All measurements were completed at the university's laboratory. 2.4. Statistical analysis After testing the data for the normal distribution using Shapiro-

Wilk tests and histograms, non-parametric distribution of data was confirmed. Significance of differences between the measurements was determined using Friedman tests (p ¼0 .05). If a significant main effect was detected, the Wilcoxon signed-rank test was applied for post hoc pair-wise comparisons of the conditions with appropriate Bonferroni adjustment. The local significance limit was set to (p ¼ 0.05/15 ¼ 0.003). Statistical analysis was conducted with commercial software (IBM SPSS Statistics 23.0). 3. Results 3.1. Muscle activity The TA (Fig. 3), PL (Fig. 3) and BF (Fig. 4) muscles showed significantly higher mean activities under the condition BP and under the conditions rearfoot stable/forefoot unstable in frontal plane and multidirectional compared with the control condition (Z [N ¼ 27] ¼ 3.700 to 4.541, p <0 .001). The PL muscle (Fig. 3) demonstrated a significantly higher mean activity under the condition forefoot stable/rearfoot unstable in frontal plane (Z [N ¼ 27] ¼ 3.219, p ¼ 0.001). The SOL (Fig. 3) was significantly more active while balancing on the BP (Z[N ¼ 27] ¼ 3.700, p < 0.001). Muscle activity of the VM (Fig. 4) was significantly increased under the conditions rearfoot stable/forefoot unstable in frontal plane and multidirectional (Z[N ¼ 27] ¼ 4.180 and 4.373, p < 0.001). Significance of differences of relative effects of mean EMGactivity (%) normalized to the control condition between unstable conditions is presented in Figs. 3 and 4 by the horizontal continuous lines. 3.2. Knee sagittal plane kinematics The average knee angles at the beginning of the balance task ranged from 15.7 (±6.0) under the control condition to 18.3 (±7.1) on the BP. The mean change of sagittal knee angle was significantly higher under the conditions rearfoot stable/forefoot unstable in frontal plane and multidirectional as compared with the other conditions (p ¼0 .001, Table 2). 3.3. Rating of perceived stability All participants stated that single-leg stance on the floor was the most stable condition (Table 3). The condition rearfoot stable/ forefoot unstable multidirectional was rated as the most unstable condition followed by the condition rearfoot stable/forefoot unstable in frontal plane. 4. Discussion The main finding was that destabilizing the forefoot in frontal plane as well as multidirectional demonstrated increased mean activation of the lower extremity muscles TA, PL, BF and VM compared with the stable control condition and the other unstable conditions. The activity of the SOL muscle was increased while balancing on the soft BP. Therefore, destabilizing the forefoot seems to be the most challenging balance task for the neuromuscular system. The increased mean change of sagittal knee angles for these conditions underlines this assumption. Compared to double leg-stance, the base of support against excursions is diminished from the space between two feet to the size of the supporting foot during single-leg stance (Liu et al., 2012). Corrective actions in the lower-extremity are induced by multijoint movements when balancing on one leg either on firm or foam surfaces (Liu et al., 2012; Riemann et al., 2003). Moreover, the

Please cite this article in press as: Alfuth, M., & Gomoll, M., Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot, Physical Therapy in Sport (2018), https://doi.org/10.1016/j.ptsp.2018.01.002

M. Alfuth, M. Gomoll / Physical Therapy in Sport xxx (2018) 1e8

5

Fig. 3. Boxplots (median of individual differences along with quartiles) demonstrating relative effects of mean activity (%) of the lower leg muscles TA (A), SOL (B) and PL (C) normalized to the control condition/floor (dotted zero line). Horizontal continuous lines represent significant differences between the unstable conditions (TA, PL: p ¼ .001; SOL p ¼ .002). Dots represent moderate outliers, asterisks represent extreme outliers.

Fig. 4. Boxplots (median of individual differences along with quartiles) demonstrating relative effects of mean activity (%) of the upper leg muscles BF (A) and VM (B) normalized to the control condition/floor (dotted zero line). Horizontal continuous lines represent significant differences between the unstable conditions (BF, VM: p ¼ .001). Dots represent moderate outliers, asterisks represent extreme outliers.

Please cite this article in press as: Alfuth, M., & Gomoll, M., Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot, Physical Therapy in Sport (2018), https://doi.org/10.1016/j.ptsp.2018.01.002

6

M. Alfuth, M. Gomoll / Physical Therapy in Sport xxx (2018) 1e8

Table 2 Inter-quartiles of mean change of knee angle in sagittal plane [ ] for the stable control condition and the unstable conditions of the Mini Stability Trainer and balance pad (FP ¼ frontal plane; MD ¼ multidirectional). Mean change of knee angle in sagittal plane [ ] Condition

Minimum

25th

Median

75th

Maximum

Control (floor) Forefoot stable/ rearfoot unstable (FP) Forefoot stable/ rearfoot unstable (MD) Rearfoot stable/ forefoot unstable (FP) Rearfoot stable/ forefoot unstable (MD) Balance Pad

0.3 0.4

2.5 2.0

3.3 3.2

3.9 4.2

8.2 7.9

0.3

2.1

3.3

5.6

9.8

0.8

3.8

6.1a

7.4

21.8

1.0

3.9

5.9

a

7.5

11.1

1.1

1.6

2.1

2.4

4.6

a

Significant difference to the control condition, the conditions forefoot stable/ rearfoot unstable and the balance pad (p ¼ 0.001).

Table 3 Rating of perceived stability of the therapy devices. Rating of perceived stability Condition Floor Forefoot stable/ rearfoot unstable (FP) Forefoot stable/ rearfoot unstable (MD) Rearfoot stable/ forefoot unstable (FP) Rearfoot stable/ forefoot unstable (MD) Balance Pad a

Level 1

Level 2

Level 3

Level 4

Level 5

Level 6

0 11a

0 12a

0 3

0 0

0 1

0

5

11

9

1

1

0

0

2

2

19a

4

0

1

0

0

5

21a

0

10

2

13a

2

0

27 0

a

Most frequently nominated.

whole body center of mass moves away from the supporting leg inducing a lateral bending (hip abduction/adduction) moment that is equilibrated at the ankle level by supination or pronation of the ankle that involves axial rotation (Liu et al., 2012). When the corrective supination and pronation at the ankle level is disturbed, especially by the destabilization of the forefoot, compensating for this bending moment may be exacerbated. Thus, an increased change of knee angle might have been a result of an increased compensatory movement strategy in response to an increased instability of the forefoot. Furthermore, the majority of lower extremity muscles might have increased activity to ensure stability of the ankle and knee joint. Sensorimotor training, where the subject needs to maintain the center of mass as quiet as possible and the ankle serves as the fixed point while balancing on an unstable surface (Freyler, Krause, Gollhofer, & Ritzmann, 2016), is considered to primarily address distal leg muscles (Rozzi, Lephart, Sterner, & Kuligowski, 1999; Taube et al., 2007). These results are partially similar to the findings of the present study, because an increased activity was only found for the lower leg muscles TA and PL under both conditions rearfoot stable/forefoot unstable and the BP, but not for the TA under the condition forefoot stable/rearfoot unstable multidirectional and the condition forefoot stable/rearfoot unstable in frontal plane. Under the conditions rearfoot stable/forefoot unstable activities of BF and VM muscles as well as mean change of sagittal knee angle were also increased. Therefore, destabilizing the forefoot seems to be a crucial factor, affecting the amount of sagittal knee joint excursions and proximal muscle activation during sensorimotor training. It was shown that the curves illustrating the ankle motion during sudden unexpected medial and lateral ankle tilts during

single-leg stance have been smoother than those describing the medial and lateral foot joint motion (Morey-Klapsing et al., 2005). However, no differences in EMG-amplitudes were found between ankle to tibia motions and forefoot to rearfoot motions. The authors concluded, that passive structures may be responsible for counteracting ankle excursions in frontal plane. During sudden destabilization a reaction of muscles within a short time interval is mainly required. However, it was found that the first notable reaction of active eversion occurred 176 ms after onset of platform tilt (Konradsen et al., 1997). This indicates that open-loop control mechanisms/preparatory activity of inversion and eversion muscles are required to control ankle excursion sufficiently (Collins & De Luca, 1993; Konradsen et al., 1997). In contrast, participants in the present study had to continuously control ankle and forefoot or rearfoot motion during the balance tasks, indicating that closed-loop/feedback control mechanisms of the ankle and foot joint movement may have dominated (Collins & De Luca, 1993; Gutierrez et al., 2009). Morey-Klapsing et al. (MoreyKlapsing et al., 2005) found that PL and TA muscle activities did not differ between medial and lateral tilts in the early response phase (0e50ms), where open-loop control mechanisms are primarily needed, but differed in the main response phase (50e200ms), where closed-loop control mechanisms may be involved. Moreover, SOL and GM muscle activities did not differ in both phases. Similarly, increased activities for the lower leg muscles TA and PL compared with GM and SOL muscles for both conditions rearfoot stable/forefoot unstable were found in the present study. This may indicate, that the sensorimotor system is able to selectively activate lower leg muscles related to medial and lateral forefoot tilting during single-leg stance on different surfaces, where closed-loop control mechanisms may be involved. An additional reason for the increased muscle activation for TA, PL, BF and VM muscles in the conditions rearfoot stable/forefoot unstable in comparison to the condition BP might have been the narrower base of support of the plates of the MST. A narrower base of support induces an increased muscle activity (Borreani et al., 2014). However, as the MST conditions forefoot stable/rearfoot unstable have the identically base of support as the MST conditions rearfoot stable/rearfoot unstable this factor seemed to play a minor role for muscle activation. It was reported, that more challenging balance conditions, i.e. foam surface, lead to increased corrective actions at the knee and hip (Riemann et al., 2003). However, in the present study the foam surface (BP) did not induce an increased mean change of sagittal knee angle compared with the control condition. Moreover, destabilizing the forefoot in frontal plane as well as multidirectional using the MST resulted in significantly increased mean change of knee angle and may have been the decisive factor for an altered balance strategy. For most muscles, activity increased from the level of most stable to less stable (Strom et al., 2016; Wolburg et al., 2016). The increased mean change of knee angles in both conditions of the present study, where the forefoot was destabilized, underlines the assumption that the knee is involved in a corrective action when a single-leg balance task becomes more challenging by destabilizing the forefoot. Consequently, muscle activities of BF and VM were higher here compared with the other unstable conditions, where a partially increased activity of the ankle encompassing muscles might have been enough for maintaining postural control. Similar to the present study, activity of the PL was higher when balancing on a wobble board with the foot placed along a frontal axis where the board tilted in medio-lateral direction inducing inversion/ eversion movement of the foot compared with balancing on an Airex pad (De Ridder et al., 2015). Borreani et al. (Borreani et al., 2014) observed the highest muscle activities for PL, TA and SOL in

Please cite this article in press as: Alfuth, M., & Gomoll, M., Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot, Physical Therapy in Sport (2018), https://doi.org/10.1016/j.ptsp.2018.01.002

M. Alfuth, M. Gomoll / Physical Therapy in Sport xxx (2018) 1e8

unipedal stance on unstable surfaces. At closer examination of their results, the SOL responded with higher activation during all conditions in unipedal stance on the soft stability trainer compared with the respective conditions using the rocker board and the stable surface. This is in line with the findings of the present study, where the SOL was mainly active on the soft BP. It leads to the assumption, that this muscle increases activity when the forefoot subsides into the pad while performing a plantarflexion. The study has some limitations. Tilting of unstable devices induced motions of the ankle and/or the different parts of the foot, i.e. forefoot and rearfoot. However, the differences of the amount of joint motions and angular velocities between these unstable conditions remained unclear. An association between the degrees of joint motions as well as angular velocities and muscle activities could not be demonstrated. A further biomechanical study using a three-dimensional foot model (Morey-Klapsing et al., 2005) would be needed. Different foot types were not determined. Furthermore, as mean change of knee angles was increased in the conditions rearfoot stable/forefoot unstable in frontal plane and multidirectional, the muscles crossing the knee joint did not operate at the same length compared with the other conditions. This might have played a role as a confounder because activation levels of the quadriceps and hamstring muscles were found to depend on different knee angles during isokinetic extension-flexion movements (Croce & Miller, 2006). As only healthy people were studied, future research should compare the acute and long-term effects of the introduced devices between healthy and clinically affected persons on muscle activation in order to identify the most suitable exercises for the respective population. 5. Conclusion The majority of lower extremity muscles seems to be more active when the forefoot is destabilized while the rearfoot is fixed during single-leg stance. The activation of the SOL muscle appears to be increased when the forefoot has to perform a plantarflexion, i.e. when balancing on the soft BP. The differences in sagittal knee joint kinematics indicate that participants used an altered balance strategy during destabilization of the forefoot. Consequently, destabilizing the forefoot using the unstable plates of the MST might be useful to address TA, PL, BF and VM muscles in order to lower the risk of initial as well as recurrent ankle sprains. Destabilizing the rearfoot is comparable to single-leg stance on a stable surface and might be useful in early phases of rehabilitation after ankle sprain. The BP might be recommended when neuromuscular deficits of the SOL should be specifically restored. Conflicts of interest We wish to confirm that there has been a material support of the study of “Ludwig Artzt GmbH” (Dornburg, Germany). Furthermore, there were no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. We confirm that we have given due consideration to the protection of intellectual property associated with this work and that there are no impediments to publication, including the timing of publication, with respect to intellectual property. In so doing we confirm that we have followed the regulations of our institutions concerning intellectual property.

7

Ethical approval The study was approved by the “Ethik-Kommission der Deut€ ln” on June 16th, 2016 (Nr. 089/2016). schen Sporthochschule Ko Acknowledgements The authors would like to thank Matthew Hoch for proofreading and helping to improve the paper as well as all participants involved in the study. References Borreani, S., Calatayud, J., Martin, J., Colado, J. C., Tella, V., & Behm, D. (2014). Exercise intensity progression for exercises performed on unstable and stable platforms based on ankle muscle activation. Gait & Posture, 39, 404e409. Braun Ferreira, L. A., Pereira, W. M., Rossi, L. P., Kerpers, I. I., Rodrigues de Paula, A., Jr., & Oliveira, C. S. (2011). Analysis of electromyographic activity of ankle muscles on stable and unstable surfaces with eyes open and closed. J Bodyw Mov Ther, 15, 496e501. Choisne, J., Hoch, M. C., Bawab, S., Alexander, I., & Ringleb, S. I. (2013). The effects of a semi-rigid ankle brace on a simulated isolated subtalar joint instability. Journal of Orthopaedic Research, 31, 1869e1875. Collins, J. J., & De Luca, C. J. (1993). Open-loop and closed-loop control of posture: A random-walk analysis of center-of-pressure trajectories. Experimental Brain Research, 95, 308e318. Cote, K. P., Brunet, M. E., Gansneder, B. M., & Shultz, S. J. (2005). Effects of pronated and supinated foot postures on static and dynamic postural stability. Journal of Athletic Training, 40, 41e46. Croce, R. V., & Miller, J. P. (2006). Angle- and velocity-specific alterations in torque and semg activity of the quadriceps and hamstrings during isokinetic extension-flexion movements. Electromyography & Clinical Neurophysiology, 46, 83e100. Culvenor, A. G., Alexander, B. C., Clark, R. A., Collins, N. J., Ageberg, E., Morris, H. G., et al. (2016). Dynamic single-leg postural control is impaired bilaterally following anterior cruciate ligament Reconstruction: Implications for reinjury risk. Journal of Orthopaedic & Sports Physical Therapy, 46, 357e364. De Mits, S., Segers, V., Woodburn, J., Elewaut, D., De Clercq, D., & Roosen, P. (2012). A clinically applicable six-segmented foot model. Journal of Orthopaedic Research, 30, 655e661. De Ridder, R., Willems, T., Vanrenterghem, J., & Roosen, P. (2015). Influence of balance surface on ankle stabilizing muscle activity in subjects with chronic ankle instability. Journal of Rehabilitation Medicine, 47, 632e638. Eils, E., & Rosenbaum, D. (2001). A multi-station proprioceptive exercise program in patients with ankle instability. Medicine & Science in Sports & Exercise, 33, 1991e1998. Fraser, J. J., Feger, M. A., & Hertel, J. (2016). Clinical commentary on midfoot and forefoot involvement in lateral ankle sprains and chronic ankle instability. Part 2: Clinical considerations. Int J Sports Phys Ther, 11, 1191e1203. Freeman, M. A. (1965). Instability of the foot after injuries to the lateral ligament of the ankle. J Bone Joint Surg Br, 47, 669e677. Freyler, K., Krause, A., Gollhofer, A., & Ritzmann, R. (2016). Specific stimuli induce specific Adaptations: Sensorimotor training vs. Reactive balance training. PLoS One, 11, e0167557. Gribble, P. A., Delahunt, E., Bleakley, C., Caulfield, B., Docherty, C. L., Fourchet, F., et al. (2013). Selection criteria for patients with chronic ankle instability in controlled research: A position statement of the international ankle Consortium. Journal of Orthopaedic & Sports Physical Therapy, 43, 585e591. Gutierrez, G. M., Kaminski, T. W., & Douex, A. T. (2009). Neuromuscular control and ankle instability. PM R, 1, 359e365. Hatton, A. L., Crossley, K. M., Clark, R. A., Whitehead, T. S., Morris, H. G., & Culvenor, A. G. (2016). Between-leg differences in challenging single-limb balance performance one year following anterior cruciate ligament reconstruction. Gait & Posture, 52, 22e25. Hertel, J., Gay, M. R., & Denegar, C. R. (2002). Differences in postural control during single-leg stance among healthy individuals with different foot types. Journal of Athletic Training, 37, 129e132. Hintermann, B. (1996). Biomechanics of the ligaments of the unstable ankle joint. Sportverletzung - Sportschaden, 10, 48e54. Hogan, K. K., Powden, C. J., & Hoch, M. C. (2016). The influence of foot posture on dorsiflexion range of motion and postural control in those with chronic ankle instability. Clinical Biomechanics, 38, 63e67. Konrad, P. (2006). The ABC of EMG: A practical introduction to kinesiological electromyography. Version 1.4 march 2006. USA: Noraxon INC. Konradsen, L., Olesen, S., & Hansen, H. M. (1998). Ankle sensorimotor control and eversion strength after acute ankle inversion injuries. The American Journal of Sports Medicine, 26, 72e77. Konradsen, L., Ravn, J. B., & Sorensen, A. I. (1993). Proprioception at the ankle: The effect of anaesthetic blockade of ligament receptors. J Bone Joint Surg Br, 75, 433e436. Konradsen, L., Voigt, M., & Hojsgaard, C. (1997). Ankle inversion injuries. The role of

Please cite this article in press as: Alfuth, M., & Gomoll, M., Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot, Physical Therapy in Sport (2018), https://doi.org/10.1016/j.ptsp.2018.01.002

8

M. Alfuth, M. Gomoll / Physical Therapy in Sport xxx (2018) 1e8

the dynamic defense mechanism. The American Journal of Sports Medicine, 25, 54e58. Liu, W., Santos, M. J., McIntire, K., Loudon, J., Goist-Foley, H., & Horton, G. (2012). Patterns of inter-joint coordination during a single-limb standing. Gait & Posture, 36, 614e618. Manter, J. T. (1941). Movements of the subtalar and transverse tarsal joint. The Anatomical Record, 80, 397e410. McGuine, T. A., Greene, J. J., Best, T., & Leverson, G. (2000). Balance as a predictor of ankle injuries in high school basketball players. Clinical Journal of Sport Medicine, 10, 239e244. McKeon, P. O., & Fourchet, F. (2015). Freeing the foot: Integrating the foot core system into rehabilitation for lower extremity injuries. Clinics in Sports Medicine, 34, 347e361. McKeon, P. O., & Hertel, J. (2008). Systematic review of postural control and lateral ankle instability, part I: Can deficits be detected with instrumented testing. Journal of Athletic Training, 43, 293e304. McKeon, P. O., Hertel, J., Bramble, D., & Davis, I. (2015). The foot core system: A new paradigm for understanding intrinsic foot muscle function. British Journal of Sports Medicine, 49, 290. Merletti, R., Botter, A., & Barone, U. (2016). Detection and conditioning of surface EMG signals. In R. Merletti, & D. Farina (Eds.), Surface electromyography: Physiology, engineering, and applications (pp. 54e90). Hoboken, New Jersey: John Wiley & Sons, Inc. Mitchell, S. L., Collins, J. J., De Luca, C. J., Burrows, A., & Lipsitz, L. A. (1995). Openloop and closed-loop postural control mechanisms in Parkinson's disease: Increased mediolateral activity during quiet standing. Neuroscience Letters, 197, 133e136. Morey-Klapsing, G., Arampatzis, A., & Bruggemann, G. P. (2005). Joint stabilising response to lateral and medial tilts. Clinical Biomechanics, 20, 517e525. Morrison, K. E., & Kaminski, T. W. (2007). Foot characteristics in association with inversion ankle injury. Journal of Athletic Training, 42, 135e142. Pfusterschmied, J., Lindinger, S., Buchecker, M., Stoggl, T., Wagner, H., & Muller, E. (2013). Effect of instability training equipment on lower limb kinematics and muscle activity. Sportverletzung - Sportschaden, 27, 28e33.

Pisani, G., Pisani, P. C., & Parino, E. (2005). Sinus tarsi syndrome and subtalar joint instability. Clinics in Podiatric Medicine and Surgery, 22, 63e77. vii. Podzielny, S., & Hennig, E. M. (1997). Restriction of foot supination by ankle braces in sudden fall situations. Clinical Biomechanics, 12, 253e258. Riemann, B. L., Myers, J. B., & Lephart, S. M. (2003). Comparison of the ankle, knee, hip, and trunk corrective action shown during single-leg stance on firm, foam, and multiaxial surfaces. Archives of Physical Medicine and Rehabilitation, 84, 90e95. Rozzi, S. L., Lephart, S. M., Sterner, R., & Kuligowski, L. (1999). Balance training for persons with functionally unstable ankles. Journal of Orthopaedic & Sports Physical Therapy, 29, 478e486. Sefton, J. M., Yarar, C., Hicks-Little, C. A., Berry, J. W., & Cordova, M. L. (2011). Six weeks of balance training improves sensorimotor function in individuals with chronic ankle instability. Journal of Orthopaedic & Sports Physical Therapy, 41, 81e89. Strom, M., Thorborg, K., Bandholm, T., Tang, L., Zebis, M., Nielsen, K., et al. (2016). Ankle joint control during single-legged balance using common balance training devices - implications for rehabilitation strategies. Int J Sports Phys Ther, 11, 388e399. Taube, W., Kullmann, N., Leukel, C., Kurz, O., Amtage, F., & Gollhofer, A. (2007). Differential reflex adaptations following sensorimotor and strength training in young elite athletes. Int J Sports Med, 28, 999e1005. Trojian, T. H., & McKeag, D. B. (2006). Single leg balance test to identify risk of ankle sprains. British Journal of Sports Medicine, 40, 610e613. discussion 613. Tsai, L. C., Yu, B., Mercer, V. S., & Gross, M. T. (2006). Comparison of different structural foot types for measures of standing postural control. Journal of Orthopaedic & Sports Physical Therapy, 36, 942e953. Verhagen, E., van der Beek, A., Twisk, J., Bouter, L., Bahr, R., & van Mechelen, W. (2004). The effect of a proprioceptive balance board training program for the prevention of ankle sprains: A prospective controlled trial. The American Journal of Sports Medicine, 32, 1385e1393. Wolburg, T., Rapp, W., Rieger, J., & Horstmann, T. (2016). Muscle activity of leg muscles during unipedal stance on therapy devices with different stability properties. Physical Therapy in Sport, 17, 58e62.

Please cite this article in press as: Alfuth, M., & Gomoll, M., Electromyographic analysis of balance exercises in single-leg stance using different instability modalities of the forefoot and rearfoot, Physical Therapy in Sport (2018), https://doi.org/10.1016/j.ptsp.2018.01.002