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Improved postural control in response to a 4-week balance training with partially unloaded bodyweight
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GAIPOS-4194; No. of Pages 6 Gait & Posture xxx (2014) xxx–xxx
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Improved postural control in response to a 4-week balance training with partially unloaded bodyweight K. Freyler *, E. Weltin, A. Gollhofer, R. Ritzmann Department of Sport and Sport Science, University of Freiburg, Germany
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 December 2013 Received in revised form 6 March 2014 Accepted 8 April 2014
Balance training (BT) is successfully implemented in therapy as a countermeasure against postural dysfunctions. However, patients suffering from motor impairments may not be able to perform balance rehabilitation with full body load. The purpose of this study was to investigate whether partial unloading leads to the same functional and neuromuscular adaptations. The impact on postural control of a 4-week BT intervention has been compared between full and partial body load. 32 subjects were randomly assigned to a CON (conventional BT) or a PART group (partially unloaded BT). BT comprised balance exercises addressing dynamic stabilization in mono- and bipedal stance. Before and after training, centre of pressure (COP) displacement and electromyographic activity of selected muscles were monitored during different balance tasks. Co-contraction index (CCI) of soleus (SOL)/tibialis (TA) was calculated. SOL H-reflexes were elicited to evaluate changes in the excitability of the spinal reflex circuitry. Adaptations in response to the training were in a similar extent for both groups: (i) after the intervention, the COP displacement was reduced (P < 0.05). This reduction was accompanied by (ii) a decreased CCI of SOL/TA (P < 0.05) and (iii) a decrease in H-reflex amplitude (P < 0.05). BT under partial unloading led to reduced COP displacements comparable to conventional BT indicating improved balance control. Moreover, decreased co-contraction of antagonistic muscles and reduced spinal excitability of the SOL motoneuron pool point towards changed postural control strategies generally observed after full body load training. Thus, BT considering partial unloading is an appropriate alternative for patients unable to conduct BT under full body load. ß 2014 Elsevier B.V. All rights reserved.
Keywords: Sensorimotor training Partial weight-bearing H-reflex Neuromuscular Rehabilitation
1. Introduction It is well known that balance training (BT) improves postural skills [1,2] and subsequently reduces the incidence of lower limb injuries [3,4] as well as decreases the risk of sustaining a fall [5,6]. As a consequence, BT is used in therapy to counteract circumstances where postural and motor control are compromised [7,8]. However, people suffering from motor impairments or reduced mobility (e.g. post-surgery, neurological diseases, the elderly) may not be able to bear their full bodyweight and thus are potentially not capable of participating in conventional intervention programmes. It could be expected that these patient groups
* Corresponding author at: Department of Sports and Sports Science, University of Freiburg, Schwarzwaldstraße 175, 79117 Freiburg, Germany. Tel.: +49 761 203 4562; fax: +49 761 203 4534. E-mail address: [email protected] (K. Freyler).
may be able to perform BT with partially unloaded bodyweight. Partial unloading of the bodyweight is already routinely applied in gait therapy to counteract neurological disorders during early stage of rehabilitation [9]. Therefore, partial body load conditions during BT could provide early recovery of the functional and neuromuscular properties as static and dynamic balance control are essential skills for daily activities [10]. It is well documented that improvements in balance performance in response to conventional BT (full bodyweight) evoke adaptations within the central nervous system (CNS, [11]). Current findings show that improved postural skills in general are associated with the plasticity of the CNS [12] and it is emphasized that spinal [13,14] and supraspinal [15,16] adaptations in particular may be responsible for the enhancement in postural control. Studies investigating the spinal reflex circuitries by means of peripheral nerve stimulation suggest that BT reduces the excitability of spinal reflexes [13,14]. The decreased spinal excitability is supposed to diminish involuntary postural oscillations and thus is believed to
http://dx.doi.org/10.1016/j.gaitpost.2014.04.186 0966-6362/ß 2014 Elsevier B.V. All rights reserved.
Please cite this article in press as: Freyler K, et al. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture (2014), http://dx.doi.org/10.1016/j.gaitpost.2014.04.186
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result in a distinct enhancement in balance performance [11]. From a functional perspective regarding the interaction between agonist and antagonist muscle groups, the enhancement in balance performance was shown to be accompanied by a decreased cocontraction [17]. More particular, a reduced co-contraction is considered to play an important role when an accurate and specific balance control is required within a demanding postural task. Taken together, adaptations of neuromuscular properties (i.e. decreased spinal excitability combined with a reduction in simultaneously activated antagonistic muscles) imply a more efficient motor control and thus are supposed to substantially contribute to the improved postural skills. From a biomechanical point of view, BT under partial unloading conditions must not necessarily evoke similar functional and neuromuscular adaptations compared to full body load BT [18]. For that purpose, this study aimed to compare adaptations of a four-week BT intervention in two subgroups training either under full or partial body load conditions. Particular interest was given in understanding the possible group specific functional and neuromuscular adaptations. It was hypothesized that (a) improvements in balance control are accompanied by (b) a decrease in co-contraction of antagonistic muscles and (c) a reduction in H-reflex amplitudes; however the improvements are expected to be more pronounced in the group that performed conventional BT. 2. Materials and methods 2.1. Subjects 32 healthy subjects (18 females, 15 males, mean age 24 2 years) participated in this study. All subjects provided written informed consent for the experiment, which was approved by the ethics committee of the University Freiburg and was in accordance with the Declaration of Helsinki. The participants were randomly assigned to either the group performing partially unloaded BT (PART, n = 16, 9 female, 8 male, age 24 2years, height 175 7 cm, weight 69 11 kg) or to the control group performing conventional BT with full body load (CON, n = 16, 9 female, 7 male, age 24 2years, height 173 10 cm, weight 70 13 kg). 2.2. Experimental design A four-week training study design was chosen to evaluate the influence of partial bodyweight unloading during BT on postural control. Centre of Pressure (COP) displacement, electromyographic activity (EMG) and H-reflex amplitudes were assessed before and after the intervention in three different test conditions which display a gradual level of difficulty from simple to complex postural tasks: bipedal stance (BS, control condition for normalization), monopedal stance (MS) on a stable surface and monopedal stance on an instable surface (MIS, spinning top). Three trials of 30 s were performed for each condition. 2.3. Training intervention All participants performed a visual feedback-based BT for a period of four weeks, with two training sessions per week separated by minimum one day rest. One session lasted 35 min and consisted of 5 min warm up, 10 min static BT and 20 min dynamic BT. During static BT subjects stood on their left leg keeping their COP (displayed on a screen, distance 2 m) as still as possible. During dynamic BT, subjects stood on both legs and traced a circled line as accurately as possible by shifting their COP in the predefined directions. Each task was performed for durations of 30 s with pauses of 30 s. The volume of BT was kept equal for both groups. The CON group performed BT with full bodyweight, whereas the PART group trained with a 60% unloading of the body’s mass [19]. Unloading was achieved by means of a bodyweight-support harness system consisting of elastic straps connected to a ceiling-mounted height-adjustable system (Fig. 1). 2.4. Outcome measures 2.4.1. Postural sway Total (COPtotal), anterior–posterior (a–p, COPap) and medial–lateral (m–l, COPml) COP displacement was determined on a force plate (AMTI, Watertown, USA) (Fig. 2). 3D ground reaction forces were sampled at 50 Hz. The participants were barefoot, placed their hands akimbo, directed their head and eyes forward and were asked to stand as still as possible. Prior to measurements each subject practiced 10 min to adapt to the instable surface.
Fig. 1. Partial unloading system: elastic straps were fixed to the subject via a climbing harness. The height-adjustable system was ceiling-mounted and extended over 7 m. The unloading of the subjects was adjusted to 40% of the bodyweight by weighing them on a scale.
2.4.2. EMG recording EMG data was obtained by placing surface electrodes (19 mm, Ag/AgCl, Ambu Blue Sensor P, Ballerup, Denmark) over m. soleus (SOL), tibialis anterior (TA) and peroneus longus (PER). Electrodes were placed in line with the direction of the underlying muscle fibres with a centre-to-centre distance of 25 mm. By shaving and light abrasion of the skin interelectrode resistance was kept below 5 kV. Signals were amplified (1000) and recorded with 1 kHz (band-pass filter 10 Hz to 1 kHz). 2.4.3. Peripheral nerve stimulation Modulation in spinal excitability of SOL was assessed by eliciting H-reflexes. The posterior tibial nerve was stimulated with 1 ms square-wave pulses using an electrical stimulator (Digitimer1, DS 7). The anode was fixed underneath the patella and the cathode was placed in the popliteal fossa. Prior to measurements, H/Mrecruitment curves were recorded during upright stance detecting the maximal Hreflex and M-wave (Mmax) [14]. For data collection, the stimulation current was adjusted to elicit H-reflexes with the size of 25% Mmax. Electrical stimulation was triggered to occur every four seconds resulting in 20 H-reflexes in each stance condition (Fig. 2). 2.4.4. Kinematics Ankle and knee angles were recorded by monoaxial electrogoniometers (Biometrics1, Gwent, UK). One goniometer was placed over the medial epicondyle of the femur (endplate attached to the shank aligned to the medial malleolus) and the other to the thigh (aligned to the greater trochanter). The second goniometer was fixed at the medial aspect of the ankle (ends attached to the axis of the foot and leg). Signals were recorded with 1 kHz and band-pass filtered (10 Hz to 1 kHz). 2.4.5. Data processing COPap and COPml was assessed and COPtotal was calculated corresponding to the Pythagoras theorem COPtotal = SDi, i = [0; 1500] with Di = [(Displacement in a–p
Please cite this article in press as: Freyler K, et al. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture (2014), http://dx.doi.org/10.1016/j.gaitpost.2014.04.186
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Fig. 2. Changes in COP movement (top) and mean H-reflex amplitudes over 20 H-reflexes (bottom, mean as solid line, SD as dotted line) during MIS of one subject of the PART group and one subject of the CON group. Both subjects showed a decrease in COP movement as well and a reduced H-reflex amplitude in response to the training.
axis)2 + (Displacement in m–l axis)2]½. Data were averaged for trials and subjects. Post values were normalized to the corresponding values of the pretest. For each of the recorded muscles, EMG signals with a length of 30 s were rectified and integrated (iEMG [mVs]). Subsequently, the mean iEMG was calculated for trials and subjects and the iEMG of MS and MIS were normalized to the corresponding iEMG of BS. To assess the simultaneous activation of antagonistic muscles, co-contraction index (CCI) of SOL/TA was calculated with the rectified and normalized EMG by means of the following equation: CCI = S[(lower EMGi/higher EMGi) (lower EMGi + higher EMGi)] for each sample point i = [0; 30000][20]. Peak-to-peak amplitudes of the H-reflexes and M-waves were calculated and averaged for each stance condition and MS and MIS were normalized to the values of BS. Regarding the kinematics, the knee flexion angle was set to zero at 1808 between the femur and the fibula. An angle of 908 between the longitudinal axis of the foot and the fibula was defined at the ankle; a plantar flexion was reflected by an angle greater than 908. For each condition, the joint angles were averaged for trials and subjects. 2.4.6. Statistics The effects of training on the dependent variables COP displacement, iEMG, CCI and H-reflex amplitudes were evaluated using a three-factor repeated-measures analyses of variance (ANOVA) group [PART vs. CON] time [pre vs. post] stance condition [MS vs. MIS]. To detect whether partially unloaded BT had an influence itself, we executed separate ANOVAs for the PART group (ANOVApart). To assess differences in joint angles, a two-factor ANOVA [time (2) group (2)] was calculated for each stance condition. The alpha level was set to 0.05. In case of significant F-values, Student’s t-tests were calculated to assess differences between pre- and post-values. Bonferroni correction was used to control for multiple testing. Statistical tests were executed by using SPSS 20.0 (SPSS, Inc., Chicago, IL, USA). Group data are presented as mean values standard deviations (M SD).
3. Results 3.1. Postural sway Changes in COPtotal displacement of two representative subjects of both groups are illustrated in Fig. 2; the grand means are shown in Fig. 3A and B. The ANOVA (P = 0.001) and ANOVApart (P = 0.003) revealed a significant time main effect, indicating a decreased sway path after the training period (PART: COPMS – 8.2 9.3 cm, COPMIS – 7.6 17.4 cm; CON: COPMS – 14.0 23.6 cm, COPMIS – 16.1 24.5 cm). The ANOVA showed no differences between groups. Regarding the different directions of postural sway, a significant time main effect could be observed in both directions for both groups (ANOVA COPap: P = 0.007; COPml: P = 0.001; Table 1 and Fig. 4). A separate training induced effect of partially unloaded BT could also be observed (ANOVApart COPap: P = 0.02; COPml: P = 0.002). 3.2. EMG activity For all recorded muscles, the ANOVA (SOL P = 0.001, TA P = 0.001, PER P = 0.005) and the ANOVApart (SOL P = 0.001, TA P = 0.001, PER P = 0.02) revealed a significant main effect for stance indicating an overall increase in EMG activity with increasing stance complexity. Furthermore, a significant time main effect in TA (ANOVA P = 0.01; ANOVApart P = 0.03) could be observed, i.e. muscular activity in TA was decreased after the intervention (Table 1). An interaction effect
Please cite this article in press as: Freyler K, et al. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture (2014), http://dx.doi.org/10.1016/j.gaitpost.2014.04.186
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BS
**
MS
*
MIS
BS
1
MS
PART
MIS
** **
MS
MIS
MS
MIS
CON
1,3
H-Reflex
D
BS
pre post
PART
1,3
0,7
160 140 120 100 80 60 40 20 0
COPtotal [cm]
pre post
H-Reflex
C
B 160 140 120 100 80 60 40 20 0
COPtotal [cm]
COPtotal [cm]
A
1
0,7
BS
CON
Fig. 3. (A) and (B) illustrate the total COP displacement for the stance conditions BS, MS and MIS. (A) shows the data of the PART group; (B) shows the data for the CON group. An increase in stance complexity (BS to MIS) results in an increase of COPtotal displacement; significantly reduced COPtotal displacements could be observed after the interventions (pre-post). In (D) and (C), COPtotal displacements (&) and H-Reflex amplitudes (~) are displayed for the PART (C) and the CON (D) group before (black) and after (grey) the interventions. For both groups the training-induced decrease in COPtotal displacement ( ) was accompanied by a reduced H-reflex sensitivity ( ). * indicates a significant difference (*P < 0.05; **P < 0.01).
of group x stance could be observed in PER (ANOVA P = 0.04). No differences between groups were observed. 3.3. CCI The ANOVA (P = 0.001) as well as the ANOVApart (P = 0.001) revealed significant differences for the factor stance; i.e. CCI was higher in MIS than in MS. Further, the ANOVA (P = 0.07) and ANOVApart (P = 0.07) revealed no significant time main effect; however values showed a declining tendency after the intervention (Table 1). No differences between groups were observed. t-test comparison for the PART group showed a significantly reduced CCI of SOL/TA during MIS (p = 0.04); t-test comparison for the CON group revealed a significantly decreased CCI of SOL/TA during MS (p = 0.04) in response to training. 3.4. H-reflex Fig. 2 illustrates the training-induced changes in H-reflex amplitude for a representative subject of each group; the grand means are illustrated in Fig. 3C and D. The ANOVA (P = 0.04) and ANOVApart (P = 0.008) showed a significant time main effect indicating a decreased H-reflex amplitude after the training period (PART: HMS 16 27% HMIS 16 58%; CON: HMS 18 25% HMIS 23 25%). No differences between groups were observed. The Mwave remained unchanged. 3.5. Kinematics In Table 1, mean values of the knee and ankle angles are displayed for the PART and the CON group. No significant differences were observed.
Table 1 Mean reduction of the COPap and COPml displacement, changes (in %) in CCI and EMG activity in regard to the pre-measurements, absolute mean iEMG values (normalized to BS) and mean values of the knee and ankle angles regarding the two measurement dates (pre vs. post). All values are displayed for the two groups (PART and CON) and the two balance tasks (MS and MIS). CON
PART MS
MIS
MS
MIS
COPap (cm) COPml (cm)
4.1 8.0* 4.6 5.0*
2.1 10.7 7.1 13.8*
5.2 8.7* 11.6 22.1*
7.3 14.8* 13.1 16.3*
CCI (%) SOL/TA EMG (%) SOL TA PER
10 43 +9 54 11 33 +4 62
20 35* +8 58 17 31* +6 46
32 36* +12 36 19 19* +12 41
34 40 +14 29 11 58 +13 63
SOL (mV) pre post
2.5 1.1 2.7 1.6
3.4 1.5 3.7 1.9
2.3 0.8 2.5 1.2
3.3 1.1 3.7 1.7
TA (mV) pre post
2.9 1.6 2.6 1.0
4.5 1.8 3.8 1.6*
3.3 2.2 2.7 1.3*
5.7 4.5 5.1 3.2
PER (mV) pre post
5.1 2.0 5.3 2.5
5.9 2.1 6.3 2.3
5.2 2.3 5.8 2.2
7.4 3.8 8.3 3.6
77 48
12 7 99
38 16
95 6 98 5
93 7 96 6
99 5 98 4
Knee (8) pre post Ankle (8) pre post
9 10 8 11 96 5 94 5
Values represent M SD. * indicate significant changes in response to the training intervention (P < 0.05). For the ankle and knee angles, no significant differences could be observed across the stance conditions. No between group differences were observed in any of the parameters.
Please cite this article in press as: Freyler K, et al. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture (2014), http://dx.doi.org/10.1016/j.gaitpost.2014.04.186
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*
120
140 120
COPml [cm]
COPml [cm]
100 90 80 70
100 80 60
60 50
**
160
110
5
pre
PART
post
40
pre
CON
post
Fig. 4. Pre and post values of the medial-lateral COP displacement from each single subject as well as the mean of all subjects (bold) during MIS for the PART (~, left graph) and the CON (&, right graph) group. Significant decrease of the mean COPml displacement over the time could be observed for both groups (*P < 0.05, **P < 0.01).
4. Discussion This study aimed to investigate differences in functional and neuromuscular adaptations after a four-week BT intervention comparing partial and full body loading. The main outcomes were that (1) the COP displacement was significantly reduced. This reduction was accompanied by (2) a decreased CCI among the encompassing ankle joint muscles and (3) a decrease of Hreflex amplitudes pointing towards a reduced spinal excitability of the SOL motoneuron-pool. Between groups, no statistical differences were observed. Hence, for the amount of 60% of unloading, this study shows for the first time that balance control adaptations are comparable in fully loaded and in partially unloaded subjects. The reduction in COP displacement after BT is well documented in literature [5,21] and is associated with an enhanced postural stability indicating an increased level of balance performance [22]. Interestingly, for MIS the decrease in COP displacement was more pronounced in m–l than in a–p direction. This finding indicates that predominantly during the difficult postural task the COPml displacement was diminished to a higher extent. This seems of considerable relevance as Lord et al. [23] have shown that the postural sway in m–l direction displayed a higher correlation with an individual risk of falling. Additionally, it is discussed that a reduction in sway path is associated with a decreased incidence of ankle injury [5] and a reduced risk of falls [24]. Underlying neuromuscular mechanisms associated with the improvements in balance performance could be indicated by a distinctly decreased level of CCI and reductions in H-reflex amplitude. Quite recently, a paper reported that a high CCI is associated with a reduced level of postural control as displayed by enlarged sway paths [17]. It is argued that a high co-contraction of antagonistic muscles increases postural rigidity by restricting the ability to react precisely to sudden perturbations [2]. Concomitant with the compromised ability to execute compensatory responses adequately, it is supposed that an enhanced co-contraction increases the risk of falling [26]. Several studies that examined the effect of BT on muscle co-contraction during balance tasks observed a decreased co-contraction after the training interventions [25,27]. It is supposed that BT has positive effects on the regulation of the task specific muscle activation which consequently results in an optimized intermuscular coordination [27].
Our results are well in line with these observations, however, insignificant P-values are assumed to result from the high standard deviations (Table 1). Thus, we conclude that BT under partial unloading leads – similarly to conventional BT – to a more efficient activation of the specific muscles involved during balance tasks. In line with previously published papers [13,15], this study provides evidence for a reduction of H-reflex amplitudes in response to training in both training subgroups (Fig. 3C and D). The decline in H-reflex amplitude was equally observed for both groups and could be caused by a variety of mechanisms: as the HReflex bypasses the muscle spindles, reduced H-reflex amplitudes after BT point towards a reduction in spinal excitability indicating a decline in Ia-transmission of the SOL motoneuron-pool [15]. Based on literature, this training induced decline in Ia-transmission could be caused by increased presynaptic inhibition [12,13,15]. According to Taube et al. [15], the increased presynaptic inhibition is most likely induced via supraspinal pathways and is associated with an improvement in balance performance by inhibition of reflexinduced oscillations in postural sway. In this regard, Chen and Zou [28] stated an inverse relation between the H-reflex amplitude and COP displacement; hence a reduction in H-reflex amplitude is associated with an increase in stance stability. Based on these findings we conclude that BT under partial unloading conditions leads to an enhanced neuromuscular control during balance tasks and thus causes adaptations within the CNS comparable to those known from conventional BT. Taken together, the present study showed that for an unloading of 60%, the training induced functional and neuromuscular changes point towards fundamental adaptations in balance strategies similar to those observed after full body load BT. For clinical use, however, this study has potential limitations. Considering that only healthy subjects were recruited, the observed effects of partially unloaded BT also need to be demonstrated in patients suffering from motor impairments (e.g. the elderly, patients with neurological diseases). However, we expect this subgroup to show similar adaptations, as in literature it is well demonstrated that impaired patients positively adapt to moderate forms of conventional BT [29,30]. Moreover, it should be considered that subjects were unloaded only during training sessions but could bear their full weight during the rest of the day. Consequently, further investigation is needed to establish partially unloaded BT as an appropriate alternative for patients
Please cite this article in press as: Freyler K, et al. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture (2014), http://dx.doi.org/10.1016/j.gaitpost.2014.04.186
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unable to perform balance rehabilitation with full body load during a certain period of time. In conclusion, this study demonstrated for the first time that partially unloaded BT revealed distinct effects in healthy subjects and made substantial contribution regarding the feasibility of such a training regimen. Hence, the combination of a partially unloaded bodyweight and BT seems to be a highly promising area of therapy, considering a fast regain in mobility for patients with neurological diseases or after injury and surgery. Acknowledgements This study was funded by the German Aerospace Centre (DLR), EADS Astrium and Nintendo of Europe GmbH. Our sponsors did not have any influence on the design, methods, subject recruitment, data collection, analysis and preparation of this paper. Conflict of interest statement We have no financial and personal relationships with other people or organisations to disclose that could have inappropriately influenced our work. The funding companies neither had an influence on the decision to submit the manuscript nor on the content of the paper. References [1] Oliveira ASC, Brito Silva P, Farina D, Kersting UG. Unilateral balance training enhances neuromuscular reactions to perturbations in the trained and contralateral limb. Gait Posture 2013;38(4):894–9. [2] Sayenko DG, Masani K, Vette AH, Alekhina MI, Popovic MR, Nakazawa K. Effects of balance training with visual feedback during mechanically unperturbed standing on postural corrective responses. Gait Posture 2012;35(2):339–44. [3] Emery CA. Effectiveness of a home-based balance-training program in reducing sports-related injuries among healthy adolescents: a cluster randomized controlled trial. Can Med Assoc J 2005;172(6):749–54. [4] Verhagen E. 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(6):1385–93. [5] Melzer I, Oddsson LI. Improving balance control and self-reported lower extremity function in community-dwelling older adults: a randomized control trial. Clin Rehabil 2013;27(3):195–206. [6] Granacher U, Gollhofer A, Strass D. Training induced adaptations in characteristics of postural reflexes in elderly men. Gait Posture 2006;24:459–66. [7] McKeon PO, Ingersoll CD, Kerrigan DC, Saliba E, Bennett BC, Hertel JA. Balance training improves function and postural control in those with chronic ankle instability. Med Sci Sports Exerc 2008;40(10):1810–9. [8] Sayenko DG, Alekhina MI, Masani K, Vette AH, Obata H, Popovic MR, et al. Positive effect of balance training with visual feedback on standing balance abilities in people with incomplete spinal cord injury. Spinal Cord 2010;48(12):886–93. [9] Trueblood PR. Partial body weight treadmill training in persons with chronic stroke. Neurorehabilitation 2001;16(3):141–53.
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Improved postural control in response to a 4-week balance training with partially unloaded bodyweight K. Freyler *, E. Weltin, A. Gollhofer, R. Ritzmann Department of Sport and Sport Science, University of Freiburg, Germany
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 December 2013 Received in revised form 6 March 2014 Accepted 8 April 2014
Balance training (BT) is successfully implemented in therapy as a countermeasure against postural dysfunctions. However, patients suffering from motor impairments may not be able to perform balance rehabilitation with full body load. The purpose of this study was to investigate whether partial unloading leads to the same functional and neuromuscular adaptations. The impact on postural control of a 4-week BT intervention has been compared between full and partial body load. 32 subjects were randomly assigned to a CON (conventional BT) or a PART group (partially unloaded BT). BT comprised balance exercises addressing dynamic stabilization in mono- and bipedal stance. Before and after training, centre of pressure (COP) displacement and electromyographic activity of selected muscles were monitored during different balance tasks. Co-contraction index (CCI) of soleus (SOL)/tibialis (TA) was calculated. SOL H-reflexes were elicited to evaluate changes in the excitability of the spinal reflex circuitry. Adaptations in response to the training were in a similar extent for both groups: (i) after the intervention, the COP displacement was reduced (P < 0.05). This reduction was accompanied by (ii) a decreased CCI of SOL/TA (P < 0.05) and (iii) a decrease in H-reflex amplitude (P < 0.05). BT under partial unloading led to reduced COP displacements comparable to conventional BT indicating improved balance control. Moreover, decreased co-contraction of antagonistic muscles and reduced spinal excitability of the SOL motoneuron pool point towards changed postural control strategies generally observed after full body load training. Thus, BT considering partial unloading is an appropriate alternative for patients unable to conduct BT under full body load. ß 2014 Elsevier B.V. All rights reserved.
Keywords: Sensorimotor training Partial weight-bearing H-reflex Neuromuscular Rehabilitation
1. Introduction It is well known that balance training (BT) improves postural skills [1,2] and subsequently reduces the incidence of lower limb injuries [3,4] as well as decreases the risk of sustaining a fall [5,6]. As a consequence, BT is used in therapy to counteract circumstances where postural and motor control are compromised [7,8]. However, people suffering from motor impairments or reduced mobility (e.g. post-surgery, neurological diseases, the elderly) may not be able to bear their full bodyweight and thus are potentially not capable of participating in conventional intervention programmes. It could be expected that these patient groups
* Corresponding author at: Department of Sports and Sports Science, University of Freiburg, Schwarzwaldstraße 175, 79117 Freiburg, Germany. Tel.: +49 761 203 4562; fax: +49 761 203 4534. E-mail address: [email protected] (K. Freyler).
may be able to perform BT with partially unloaded bodyweight. Partial unloading of the bodyweight is already routinely applied in gait therapy to counteract neurological disorders during early stage of rehabilitation [9]. Therefore, partial body load conditions during BT could provide early recovery of the functional and neuromuscular properties as static and dynamic balance control are essential skills for daily activities [10]. It is well documented that improvements in balance performance in response to conventional BT (full bodyweight) evoke adaptations within the central nervous system (CNS, [11]). Current findings show that improved postural skills in general are associated with the plasticity of the CNS [12] and it is emphasized that spinal [13,14] and supraspinal [15,16] adaptations in particular may be responsible for the enhancement in postural control. Studies investigating the spinal reflex circuitries by means of peripheral nerve stimulation suggest that BT reduces the excitability of spinal reflexes [13,14]. The decreased spinal excitability is supposed to diminish involuntary postural oscillations and thus is believed to
http://dx.doi.org/10.1016/j.gaitpost.2014.04.186 0966-6362/ß 2014 Elsevier B.V. All rights reserved.
Please cite this article in press as: Freyler K, et al. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture (2014), http://dx.doi.org/10.1016/j.gaitpost.2014.04.186
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result in a distinct enhancement in balance performance [11]. From a functional perspective regarding the interaction between agonist and antagonist muscle groups, the enhancement in balance performance was shown to be accompanied by a decreased cocontraction [17]. More particular, a reduced co-contraction is considered to play an important role when an accurate and specific balance control is required within a demanding postural task. Taken together, adaptations of neuromuscular properties (i.e. decreased spinal excitability combined with a reduction in simultaneously activated antagonistic muscles) imply a more efficient motor control and thus are supposed to substantially contribute to the improved postural skills. From a biomechanical point of view, BT under partial unloading conditions must not necessarily evoke similar functional and neuromuscular adaptations compared to full body load BT [18]. For that purpose, this study aimed to compare adaptations of a four-week BT intervention in two subgroups training either under full or partial body load conditions. Particular interest was given in understanding the possible group specific functional and neuromuscular adaptations. It was hypothesized that (a) improvements in balance control are accompanied by (b) a decrease in co-contraction of antagonistic muscles and (c) a reduction in H-reflex amplitudes; however the improvements are expected to be more pronounced in the group that performed conventional BT. 2. Materials and methods 2.1. Subjects 32 healthy subjects (18 females, 15 males, mean age 24 2 years) participated in this study. All subjects provided written informed consent for the experiment, which was approved by the ethics committee of the University Freiburg and was in accordance with the Declaration of Helsinki. The participants were randomly assigned to either the group performing partially unloaded BT (PART, n = 16, 9 female, 8 male, age 24 2years, height 175 7 cm, weight 69 11 kg) or to the control group performing conventional BT with full body load (CON, n = 16, 9 female, 7 male, age 24 2years, height 173 10 cm, weight 70 13 kg). 2.2. Experimental design A four-week training study design was chosen to evaluate the influence of partial bodyweight unloading during BT on postural control. Centre of Pressure (COP) displacement, electromyographic activity (EMG) and H-reflex amplitudes were assessed before and after the intervention in three different test conditions which display a gradual level of difficulty from simple to complex postural tasks: bipedal stance (BS, control condition for normalization), monopedal stance (MS) on a stable surface and monopedal stance on an instable surface (MIS, spinning top). Three trials of 30 s were performed for each condition. 2.3. Training intervention All participants performed a visual feedback-based BT for a period of four weeks, with two training sessions per week separated by minimum one day rest. One session lasted 35 min and consisted of 5 min warm up, 10 min static BT and 20 min dynamic BT. During static BT subjects stood on their left leg keeping their COP (displayed on a screen, distance 2 m) as still as possible. During dynamic BT, subjects stood on both legs and traced a circled line as accurately as possible by shifting their COP in the predefined directions. Each task was performed for durations of 30 s with pauses of 30 s. The volume of BT was kept equal for both groups. The CON group performed BT with full bodyweight, whereas the PART group trained with a 60% unloading of the body’s mass [19]. Unloading was achieved by means of a bodyweight-support harness system consisting of elastic straps connected to a ceiling-mounted height-adjustable system (Fig. 1). 2.4. Outcome measures 2.4.1. Postural sway Total (COPtotal), anterior–posterior (a–p, COPap) and medial–lateral (m–l, COPml) COP displacement was determined on a force plate (AMTI, Watertown, USA) (Fig. 2). 3D ground reaction forces were sampled at 50 Hz. The participants were barefoot, placed their hands akimbo, directed their head and eyes forward and were asked to stand as still as possible. Prior to measurements each subject practiced 10 min to adapt to the instable surface.
Fig. 1. Partial unloading system: elastic straps were fixed to the subject via a climbing harness. The height-adjustable system was ceiling-mounted and extended over 7 m. The unloading of the subjects was adjusted to 40% of the bodyweight by weighing them on a scale.
2.4.2. EMG recording EMG data was obtained by placing surface electrodes (19 mm, Ag/AgCl, Ambu Blue Sensor P, Ballerup, Denmark) over m. soleus (SOL), tibialis anterior (TA) and peroneus longus (PER). Electrodes were placed in line with the direction of the underlying muscle fibres with a centre-to-centre distance of 25 mm. By shaving and light abrasion of the skin interelectrode resistance was kept below 5 kV. Signals were amplified (1000) and recorded with 1 kHz (band-pass filter 10 Hz to 1 kHz). 2.4.3. Peripheral nerve stimulation Modulation in spinal excitability of SOL was assessed by eliciting H-reflexes. The posterior tibial nerve was stimulated with 1 ms square-wave pulses using an electrical stimulator (Digitimer1, DS 7). The anode was fixed underneath the patella and the cathode was placed in the popliteal fossa. Prior to measurements, H/Mrecruitment curves were recorded during upright stance detecting the maximal Hreflex and M-wave (Mmax) [14]. For data collection, the stimulation current was adjusted to elicit H-reflexes with the size of 25% Mmax. Electrical stimulation was triggered to occur every four seconds resulting in 20 H-reflexes in each stance condition (Fig. 2). 2.4.4. Kinematics Ankle and knee angles were recorded by monoaxial electrogoniometers (Biometrics1, Gwent, UK). One goniometer was placed over the medial epicondyle of the femur (endplate attached to the shank aligned to the medial malleolus) and the other to the thigh (aligned to the greater trochanter). The second goniometer was fixed at the medial aspect of the ankle (ends attached to the axis of the foot and leg). Signals were recorded with 1 kHz and band-pass filtered (10 Hz to 1 kHz). 2.4.5. Data processing COPap and COPml was assessed and COPtotal was calculated corresponding to the Pythagoras theorem COPtotal = SDi, i = [0; 1500] with Di = [(Displacement in a–p
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Fig. 2. Changes in COP movement (top) and mean H-reflex amplitudes over 20 H-reflexes (bottom, mean as solid line, SD as dotted line) during MIS of one subject of the PART group and one subject of the CON group. Both subjects showed a decrease in COP movement as well and a reduced H-reflex amplitude in response to the training.
axis)2 + (Displacement in m–l axis)2]½. Data were averaged for trials and subjects. Post values were normalized to the corresponding values of the pretest. For each of the recorded muscles, EMG signals with a length of 30 s were rectified and integrated (iEMG [mVs]). Subsequently, the mean iEMG was calculated for trials and subjects and the iEMG of MS and MIS were normalized to the corresponding iEMG of BS. To assess the simultaneous activation of antagonistic muscles, co-contraction index (CCI) of SOL/TA was calculated with the rectified and normalized EMG by means of the following equation: CCI = S[(lower EMGi/higher EMGi) (lower EMGi + higher EMGi)] for each sample point i = [0; 30000][20]. Peak-to-peak amplitudes of the H-reflexes and M-waves were calculated and averaged for each stance condition and MS and MIS were normalized to the values of BS. Regarding the kinematics, the knee flexion angle was set to zero at 1808 between the femur and the fibula. An angle of 908 between the longitudinal axis of the foot and the fibula was defined at the ankle; a plantar flexion was reflected by an angle greater than 908. For each condition, the joint angles were averaged for trials and subjects. 2.4.6. Statistics The effects of training on the dependent variables COP displacement, iEMG, CCI and H-reflex amplitudes were evaluated using a three-factor repeated-measures analyses of variance (ANOVA) group [PART vs. CON] time [pre vs. post] stance condition [MS vs. MIS]. To detect whether partially unloaded BT had an influence itself, we executed separate ANOVAs for the PART group (ANOVApart). To assess differences in joint angles, a two-factor ANOVA [time (2) group (2)] was calculated for each stance condition. The alpha level was set to 0.05. In case of significant F-values, Student’s t-tests were calculated to assess differences between pre- and post-values. Bonferroni correction was used to control for multiple testing. Statistical tests were executed by using SPSS 20.0 (SPSS, Inc., Chicago, IL, USA). Group data are presented as mean values standard deviations (M SD).
3. Results 3.1. Postural sway Changes in COPtotal displacement of two representative subjects of both groups are illustrated in Fig. 2; the grand means are shown in Fig. 3A and B. The ANOVA (P = 0.001) and ANOVApart (P = 0.003) revealed a significant time main effect, indicating a decreased sway path after the training period (PART: COPMS – 8.2 9.3 cm, COPMIS – 7.6 17.4 cm; CON: COPMS – 14.0 23.6 cm, COPMIS – 16.1 24.5 cm). The ANOVA showed no differences between groups. Regarding the different directions of postural sway, a significant time main effect could be observed in both directions for both groups (ANOVA COPap: P = 0.007; COPml: P = 0.001; Table 1 and Fig. 4). A separate training induced effect of partially unloaded BT could also be observed (ANOVApart COPap: P = 0.02; COPml: P = 0.002). 3.2. EMG activity For all recorded muscles, the ANOVA (SOL P = 0.001, TA P = 0.001, PER P = 0.005) and the ANOVApart (SOL P = 0.001, TA P = 0.001, PER P = 0.02) revealed a significant main effect for stance indicating an overall increase in EMG activity with increasing stance complexity. Furthermore, a significant time main effect in TA (ANOVA P = 0.01; ANOVApart P = 0.03) could be observed, i.e. muscular activity in TA was decreased after the intervention (Table 1). An interaction effect
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BS
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Fig. 3. (A) and (B) illustrate the total COP displacement for the stance conditions BS, MS and MIS. (A) shows the data of the PART group; (B) shows the data for the CON group. An increase in stance complexity (BS to MIS) results in an increase of COPtotal displacement; significantly reduced COPtotal displacements could be observed after the interventions (pre-post). In (D) and (C), COPtotal displacements (&) and H-Reflex amplitudes (~) are displayed for the PART (C) and the CON (D) group before (black) and after (grey) the interventions. For both groups the training-induced decrease in COPtotal displacement ( ) was accompanied by a reduced H-reflex sensitivity ( ). * indicates a significant difference (*P < 0.05; **P < 0.01).
of group x stance could be observed in PER (ANOVA P = 0.04). No differences between groups were observed. 3.3. CCI The ANOVA (P = 0.001) as well as the ANOVApart (P = 0.001) revealed significant differences for the factor stance; i.e. CCI was higher in MIS than in MS. Further, the ANOVA (P = 0.07) and ANOVApart (P = 0.07) revealed no significant time main effect; however values showed a declining tendency after the intervention (Table 1). No differences between groups were observed. t-test comparison for the PART group showed a significantly reduced CCI of SOL/TA during MIS (p = 0.04); t-test comparison for the CON group revealed a significantly decreased CCI of SOL/TA during MS (p = 0.04) in response to training. 3.4. H-reflex Fig. 2 illustrates the training-induced changes in H-reflex amplitude for a representative subject of each group; the grand means are illustrated in Fig. 3C and D. The ANOVA (P = 0.04) and ANOVApart (P = 0.008) showed a significant time main effect indicating a decreased H-reflex amplitude after the training period (PART: HMS 16 27% HMIS 16 58%; CON: HMS 18 25% HMIS 23 25%). No differences between groups were observed. The Mwave remained unchanged. 3.5. Kinematics In Table 1, mean values of the knee and ankle angles are displayed for the PART and the CON group. No significant differences were observed.
Table 1 Mean reduction of the COPap and COPml displacement, changes (in %) in CCI and EMG activity in regard to the pre-measurements, absolute mean iEMG values (normalized to BS) and mean values of the knee and ankle angles regarding the two measurement dates (pre vs. post). All values are displayed for the two groups (PART and CON) and the two balance tasks (MS and MIS). CON
PART MS
MIS
MS
MIS
COPap (cm) COPml (cm)
4.1 8.0* 4.6 5.0*
2.1 10.7 7.1 13.8*
5.2 8.7* 11.6 22.1*
7.3 14.8* 13.1 16.3*
CCI (%) SOL/TA EMG (%) SOL TA PER
10 43 +9 54 11 33 +4 62
20 35* +8 58 17 31* +6 46
32 36* +12 36 19 19* +12 41
34 40 +14 29 11 58 +13 63
SOL (mV) pre post
2.5 1.1 2.7 1.6
3.4 1.5 3.7 1.9
2.3 0.8 2.5 1.2
3.3 1.1 3.7 1.7
TA (mV) pre post
2.9 1.6 2.6 1.0
4.5 1.8 3.8 1.6*
3.3 2.2 2.7 1.3*
5.7 4.5 5.1 3.2
PER (mV) pre post
5.1 2.0 5.3 2.5
5.9 2.1 6.3 2.3
5.2 2.3 5.8 2.2
7.4 3.8 8.3 3.6
77 48
12 7 99
38 16
95 6 98 5
93 7 96 6
99 5 98 4
Knee (8) pre post Ankle (8) pre post
9 10 8 11 96 5 94 5
Values represent M SD. * indicate significant changes in response to the training intervention (P < 0.05). For the ankle and knee angles, no significant differences could be observed across the stance conditions. No between group differences were observed in any of the parameters.
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Fig. 4. Pre and post values of the medial-lateral COP displacement from each single subject as well as the mean of all subjects (bold) during MIS for the PART (~, left graph) and the CON (&, right graph) group. Significant decrease of the mean COPml displacement over the time could be observed for both groups (*P < 0.05, **P < 0.01).
4. Discussion This study aimed to investigate differences in functional and neuromuscular adaptations after a four-week BT intervention comparing partial and full body loading. The main outcomes were that (1) the COP displacement was significantly reduced. This reduction was accompanied by (2) a decreased CCI among the encompassing ankle joint muscles and (3) a decrease of Hreflex amplitudes pointing towards a reduced spinal excitability of the SOL motoneuron-pool. Between groups, no statistical differences were observed. Hence, for the amount of 60% of unloading, this study shows for the first time that balance control adaptations are comparable in fully loaded and in partially unloaded subjects. The reduction in COP displacement after BT is well documented in literature [5,21] and is associated with an enhanced postural stability indicating an increased level of balance performance [22]. Interestingly, for MIS the decrease in COP displacement was more pronounced in m–l than in a–p direction. This finding indicates that predominantly during the difficult postural task the COPml displacement was diminished to a higher extent. This seems of considerable relevance as Lord et al. [23] have shown that the postural sway in m–l direction displayed a higher correlation with an individual risk of falling. Additionally, it is discussed that a reduction in sway path is associated with a decreased incidence of ankle injury [5] and a reduced risk of falls [24]. Underlying neuromuscular mechanisms associated with the improvements in balance performance could be indicated by a distinctly decreased level of CCI and reductions in H-reflex amplitude. Quite recently, a paper reported that a high CCI is associated with a reduced level of postural control as displayed by enlarged sway paths [17]. It is argued that a high co-contraction of antagonistic muscles increases postural rigidity by restricting the ability to react precisely to sudden perturbations [2]. Concomitant with the compromised ability to execute compensatory responses adequately, it is supposed that an enhanced co-contraction increases the risk of falling [26]. Several studies that examined the effect of BT on muscle co-contraction during balance tasks observed a decreased co-contraction after the training interventions [25,27]. It is supposed that BT has positive effects on the regulation of the task specific muscle activation which consequently results in an optimized intermuscular coordination [27].
Our results are well in line with these observations, however, insignificant P-values are assumed to result from the high standard deviations (Table 1). Thus, we conclude that BT under partial unloading leads – similarly to conventional BT – to a more efficient activation of the specific muscles involved during balance tasks. In line with previously published papers [13,15], this study provides evidence for a reduction of H-reflex amplitudes in response to training in both training subgroups (Fig. 3C and D). The decline in H-reflex amplitude was equally observed for both groups and could be caused by a variety of mechanisms: as the HReflex bypasses the muscle spindles, reduced H-reflex amplitudes after BT point towards a reduction in spinal excitability indicating a decline in Ia-transmission of the SOL motoneuron-pool [15]. Based on literature, this training induced decline in Ia-transmission could be caused by increased presynaptic inhibition [12,13,15]. According to Taube et al. [15], the increased presynaptic inhibition is most likely induced via supraspinal pathways and is associated with an improvement in balance performance by inhibition of reflexinduced oscillations in postural sway. In this regard, Chen and Zou [28] stated an inverse relation between the H-reflex amplitude and COP displacement; hence a reduction in H-reflex amplitude is associated with an increase in stance stability. Based on these findings we conclude that BT under partial unloading conditions leads to an enhanced neuromuscular control during balance tasks and thus causes adaptations within the CNS comparable to those known from conventional BT. Taken together, the present study showed that for an unloading of 60%, the training induced functional and neuromuscular changes point towards fundamental adaptations in balance strategies similar to those observed after full body load BT. For clinical use, however, this study has potential limitations. Considering that only healthy subjects were recruited, the observed effects of partially unloaded BT also need to be demonstrated in patients suffering from motor impairments (e.g. the elderly, patients with neurological diseases). However, we expect this subgroup to show similar adaptations, as in literature it is well demonstrated that impaired patients positively adapt to moderate forms of conventional BT [29,30]. Moreover, it should be considered that subjects were unloaded only during training sessions but could bear their full weight during the rest of the day. Consequently, further investigation is needed to establish partially unloaded BT as an appropriate alternative for patients
Please cite this article in press as: Freyler K, et al. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture (2014), http://dx.doi.org/10.1016/j.gaitpost.2014.04.186
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unable to perform balance rehabilitation with full body load during a certain period of time. In conclusion, this study demonstrated for the first time that partially unloaded BT revealed distinct effects in healthy subjects and made substantial contribution regarding the feasibility of such a training regimen. Hence, the combination of a partially unloaded bodyweight and BT seems to be a highly promising area of therapy, considering a fast regain in mobility for patients with neurological diseases or after injury and surgery. Acknowledgements This study was funded by the German Aerospace Centre (DLR), EADS Astrium and Nintendo of Europe GmbH. Our sponsors did not have any influence on the design, methods, subject recruitment, data collection, analysis and preparation of this paper. Conflict of interest statement We have no financial and personal relationships with other people or organisations to disclose that could have inappropriately influenced our work. The funding companies neither had an influence on the decision to submit the manuscript nor on the content of the paper. References [1] Oliveira ASC, Brito Silva P, Farina D, Kersting UG. Unilateral balance training enhances neuromuscular reactions to perturbations in the trained and contralateral limb. Gait Posture 2013;38(4):894–9. [2] Sayenko DG, Masani K, Vette AH, Alekhina MI, Popovic MR, Nakazawa K. Effects of balance training with visual feedback during mechanically unperturbed standing on postural corrective responses. Gait Posture 2012;35(2):339–44. [3] Emery CA. Effectiveness of a home-based balance-training program in reducing sports-related injuries among healthy adolescents: a cluster randomized controlled trial. Can Med Assoc J 2005;172(6):749–54. [4] Verhagen E. 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(6):1385–93. [5] Melzer I, Oddsson LI. Improving balance control and self-reported lower extremity function in community-dwelling older adults: a randomized control trial. Clin Rehabil 2013;27(3):195–206. [6] Granacher U, Gollhofer A, Strass D. Training induced adaptations in characteristics of postural reflexes in elderly men. Gait Posture 2006;24:459–66. [7] McKeon PO, Ingersoll CD, Kerrigan DC, Saliba E, Bennett BC, Hertel JA. Balance training improves function and postural control in those with chronic ankle instability. Med Sci Sports Exerc 2008;40(10):1810–9. [8] Sayenko DG, Alekhina MI, Masani K, Vette AH, Obata H, Popovic MR, et al. Positive effect of balance training with visual feedback on standing balance abilities in people with incomplete spinal cord injury. Spinal Cord 2010;48(12):886–93. [9] Trueblood PR. Partial body weight treadmill training in persons with chronic stroke. Neurorehabilitation 2001;16(3):141–53.
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Please cite this article in press as: Freyler K, et al. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture (2014), http://dx.doi.org/10.1016/j.gaitpost.2014.04.186