Research in Developmental Disabilities 35 (2014) 1782–1788
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Postural adaptation during arm raising in children with and without unilateral cerebral palsy Annick Ledebt *, Geert J.P. Savelsbergh Research Institute MOVE, Faculty of Human Movement Sciences, VU University Amsterdam, Van Der Boechorststraat 9, Amsterdam 1081 BT, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 October 2013 Received in revised form 10 February 2014 Accepted 14 February 2014 Available online 23 March 2014
Postural sway during arm movements were related to the size of the base of support (BOS) and the limits of stability (LOS) of children with unilateral cerebral palsy (USCP) and typically developing (TD) children. For half of the trials the mechanical disturbance due to the rapid arm movement was increased by attaching small weights at the wrists. The participants stood with both feet on a large force plate, which recorded the displacements of the center of pressure (CoP). The results showed that in the children with USCP the LOS forward and toward the non-dominant (more-affected) side were smaller than in the TD children whereas the LOS backward and toward the dominant (less-affected) side did not differ between the two groups. When rapidly moving the arms the children with USCP swayed over a larger portion of their base of support in the forward direction and toward their more-affected side. In addition, the maximal sway toward the more-affected side during arm movement exceeded the LOS while balance was maintained. These effects increased when the movements were performed with the weights at the wrists. These results show that an area of permissible sway, which was not spontaneously explored during the leaning task, was required to maintain balance during the supra-postural task. Training to enlarge the LOS that includes weight shifts toward the more-affected side might reduce the area of the BOS that is self-perceived as less secure. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Congenital hemiparesis Balance Postural adjustments Center of pressure Limits of stability Base of support
1. Introduction Poor postural control has been suggested to be one of the underlying factors to the frequent abnormal motor development in children with cerebral palsy (Roncesvalles et al., 2000). Functional level of children with cerebral palsy is ranged from independent walking with minimal walking aids (e.g., ankle–foot ortheses) to wheelchair bounded mobility. Although children with unilateral cerebral palsy (UCP) are usually high functioning and able to stand and walk independently they still encounter problems during stance when rapid weight shifts are required in preparation (Stackhouse et al., 2006) or in reaction to a perturbation (Woollacott et al., 2005). During quiet standing, children with UCP exhibit greater and more regular sway than typically developing children (Donker et al., 2008). These results have been viewed as the dynamical signature of poor postural control in children with UCP during quiet standing. Quiet standing is rarely maintained for its own sake but instead facilitates the performance of daily suprapostural tasks like visual tasks and voluntary movements of the upper limbs. Many studies have shown that in adults and typically developing children postural
* Corresponding author. Tel.: +31 20 5988462; fax: +31 20 5988529. E-mail address: [email protected] (A. Ledebt). http://dx.doi.org/10.1016/j.ridd.2014.02.007 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
A. Ledebt, G.J.P. Savelsbergh / Research in Developmental Disabilities 35 (2014) 1782–1788
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adjustments contribute to the preparation and execution of arm movements. As the movements of one or two arms contribute to the displacement of the center of mass, the position of the center of pressure (COP) has to be adjusted accordingly in order to maintain equilibrium (Bouisset & Zattara, 1987). The postural adjustments counteract the destabilizing effect of the arm movements which increases when additional constraints are involved such as extra load at the arm (Hay & Redon, 2001). The potentially destabilizing effect of such arm movements on bipedal stance is also related to the size of the area of functional postural sway. The borders of this area, the limits of stability (LOS), correspond to the region of transition from bipedal stance to stepping (Duarte & Zatsiorsky, 2002). The LOS area is commonly smaller than the base of support as defined by the geometry of the feet (BOS) and is usually evaluated for different leaning orientations (Duarte and Zatsiorsky, 2002; Forth et al., 2011). The results in adults showed that spatial variability of the postural sway increased toward the LOS when leaning increased while both feet maintained full contact with the ground. In children with cerebral palsy only preparatory adjustments to self-paced arm movement have been reported (Tomita et al., 2010) while it is still unclear how postural adjustments unfold during arm movements as a function of the BOS and the LOS. The aim of the present study was to analyze the postural adaptation during unilateral and bilateral rapid arm movement and to relate these postural shifts to the size of the base of support (BOS) and to the limits of support (LOS). Rapid movements and increased inertia (small loads at the wrists) were used to investigate the postural reactions when perturbation forces due to movements are maximized. Although the most relevant direction to analyze with respect to this task was the forward direction (Bouisset & Zattara, 1987), backward sway and sway toward the dominant and non-dominant side might reveal asymmetrical behavior in individuals with USCP. Therefore the study analyzed the global outcome of the adaptation as reflected in the shifts of the COP in relation to functional limits of standing posture defined as the base of support and the limits of stability. We expected that individuals with USCP show smaller limits of stability than TD children specifically along the medio-lateral axis in relation to the weakness of their more-affected leg. As a consequence it was expected that during arm movements the maximum postural sway would be closer to the LOS in the children with CP than in the TD group. This effect was expected to be enhanced in higher disturbing arm movements, i.e. during bilateral movements and when a small weight was added at the wrists. 2. Methods 2.1. Participants Six children with congenital hemiplegia and six typically developing children without known motor impairments participated in the experiment (see Table 1). All children with USCP could stand and walk independently in accordance with the highest functional mobility level of the Gross Motor Functioning Classification System (GMFCS level I). Their gross motor functioning was further documented according to the ability to jump (starting and ending on both feet) and to hop (small jump starting and ending on the same foot) on one and the other side (see Table 1). All children were able to understand and follow the instructions and to execute the arm raising task without restriction or pain. One child with USCP was using an ankle–foot orthesis on a daily basis. All children and their parents gave their informed consent prior to participation. The experiment was carried out in compliance with the Helsinki Declaration and was endorsed by the University Medical Centre Amsterdam. 2.2. Procedure and apparatus Participants stood upright on a 1 m 1 m custom-made strain gauge force plate (sampling rate 100 Hz). Their feet were placed parallel to the anterior–posterior axis of the force plate and the distance between the feet corresponded to pelvis width. Children wore their own shoes, including ankle–foot ortheses when necessary (only child OT) in order to correspond Table 1 Participants’ characteristics. Participant
Group
Height (cm)
Gender
Age (years)
Non-dominant/ affected side
Jump (two legs)
Hop on non-dom. leg
Hop on dom. leg
ES NC AE OT NK NJ EM ER OT TB ND YG
TD TD TD TD TD TD CP CP CP CP CP CP
1140 1150 1360 1410 1440 1430 1130 1140 1160 1340 1440 1510
F M F M F M M M M F M F
5 6 7 9 9 11 5 6 6 8 9 11
L L L L L L R R La R L R
Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes
Yes Yes Yes Yes Yes Yes No No No No No No
Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes Yes
a
Ankle–foot orthosis on affected side.
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to what they experienced in daily life. The positioning of the feet on the floor was drawn on a paper fixed to the force plate. This positioning was then maintained for the different tasks, which included voluntary leaning and arm raising while standing. The procedure followed during the leaning trials already presented elsewhere (Ledebt et al., 2005) and used a visual feedback of the COP displayed on a screen in front of the participant. A dot corresponding to the COP was visible and was moving online with the weight shifts of the child. The child was instructed to slowly move the dot in order to reach visual targets while keeping both feet completely on the ground and encouraged to use an ankle strategy (‘‘move as a block’’) rather than a hip or a mixed strategy. The targets appeared on the screen along the antero-posterior and medio-lateral axes at increasing distances from the neutral position of the COP. This way the child was motivated to lean as far as possible forward, backward, on the dominant (non-affected) leg and on the non-dominant (affected) leg. Time was given to experience the effect of own movements on the screen before the recordings were made and lasted not longer than a few minutes. The amplitude of the largest sway in each of the four directions was measured from the force plate data. For the arm raising task the children had to quickly raise one or both arms toward light emitting diodes (LED) placed in front of the shoulders after the LED turned on (right or left arm moving after respectively switching on the right or left LED and both arms when both LEDs switched on). The end position of the arms was horizontal and had to be maintained a few seconds (when LED switched off). A small uniaxial accelerometer (ICSensors 3145-002, piezoresistive sensor, linearity range: 2 g) was attached at each wrist in order to detect the beginning and the end of the arm movement. The signal of the accelerometer contains a component of the gravitational acceleration and a component of the inertial acceleration: in the absence of movement the accelerometer signal yielded inclination information while during movement this information was combined with acceleration information. During a few trying out trials it was checked that the child was able to move rapidly at least within a second between start and end position. Six conditions were applied corresponding to a fully crossed design including two factors: three arm conditions (unilateral dominant, unilateral non-dominant and bilateral) and two weight conditions (with and without addition weight at the wrists). The weight corresponded to 2% of participant’s weight at each wrist. A total of 30 arm raising trials were presented in two separate blocks, one block with and one block without weights. The order of these two blocks was counterbalanced across participants. Within each block, the 15 trials (3 arm conditions and 5 trials per conditions) were randomly presented. 2.3. Data analysis Prior to all analyses, the mean was subtracted from medio-lateral and anteroposterior CoP trajectories. The resulting time series were then filtered (second-order low-pass Butterworth filter, cut-off frequency 12.5 Hz). The maximum amplitude of the CoP trajectories along both axes was calculated for the leaning and the arm raising trials. During the leaning trials the maximum forward, backward, toward the paretic/non-dominant and toward the non-paretic/dominant side displacements were considered when maintained at least during one second. During the arm raising trials the maximum displacement in the same four directions were considered when occurring during the time the arm was moving. The beginning and the end of the arm movement were indicated by the wrist accelerometer signals (see Fig. 1). The baseline level of CoP position was calculated as the mean position of the CoP between 400 ms and 200 ms before movement onset. In addition to the absolute values of the maximum amplitudes two indexes were computed for the leaning trials and the arm raising trials respectively. As a large range of feet length in both groups of children was expected (due to the large age ranges), the maximum sway were first scaled to with respect to the BOS. The forward and backward LOS were scaled to the subject’s base of support (BOS) length as measured on the paper fixed on the force plate whereas the LOS toward the affected/non-dominant and toward the non-affected/dominant side were scaled to the width of the base of support (LOS/ BOS ratio). The width of the BOS was calculate as the average of the largest distance (usually at toes level) and the shortest distance (usually located at heel level) of the outer limits of the BOS. An identical procedure was used to scale the maximum shifts measured during arm movement to the BOS (expressed in percentage). Maximum shifts during arm movement were also scaled to the corresponding LOS for each of the four directions (expressed in percentage). The differences between children with CP and the TD children for BOS length and width and for the absolute and relative LOS (in all four directions) were analyzed by a Mann–Whitney U test. For each sway direction, the absolute and relative maximum shifts during arm raising were analyzed by a three-way 2 3 2 (group arm weight) analysis of variance, with repeated measures on the last two factors. Data are expressed as mean SD and statistical significance was accepted at p < 0.05. A Greenhouse–Geisser correction was applied when the underlying assumption of homogeneity was violated. 3. Results 3.1. CoP shifts during voluntary leaning Although on the average the base length and width did not differ between the two groups, base length maximum values indicated that the variability in the TD group was larger than in the CP group (Table 2). The absolute and relative LOS in the forward and non-dominant/affected direction was significantly smaller in the CP group than in the TD group and failed to be significant for the two other directions (Fig. 2).
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Fig. 1. Typical postural sway during the execution of a unilateral arm movement with the dominant arm of this participant (right arm). On the left, from top to bottom: displacement of the center of pressure along the sagittal axis (CoPx) and the medio-lateral axis (CoPy) and tangential acceleration recorded at the wrist (Acc.). Time zero represents the onset of arm movement indicated by an increase of acceleration followed by a decrease before arm stabilizes in the new position. The maximum displacement of the CoP was measured between the start and the end of the movement in four directions backward (CoPmax back), forward (CoPmax forw), on the dominant side (CoPmax dom) and the non-dominant side (CoPmax non-dom). The vertical bar on the bottom line indicates the moment the visual signal for the start of the movement turned on (LED). On the right: the same antero-posterior and medio-lateral displacements of the CoP are represented without the time line.
Table 2 Base of support and limits of stability. Mean (SD) Base length (m) TD CP Base width (m) TD CP LOS Forward (m) TD CP LOS Forward/BOS (%) TD CP LOS Backward (m) TD CP LOS Backward/BOS (%) TD CP LOS Dominant (m) TD CP LOS Dom/BOS (%) TD CP LOS Non-Dominant (m) TD CP LOS Non-Dom/BOS (%) TD CP
Min
Max
Mann–Whitney U
0.255 (0.665) 0.243 (0.326)
0.19 0.20
0.36 0.28
ns
0.226 (0.186) 0.225 (0.32)
0.20 0.20
0.25 0.27
ns
0.055 (0.014) 0.037 (0.008)
0.040 0.030
0.070 0.050
4.5 (p = .026)
24.3 (5.7) 16.4 (3.4) 0.036 (0.022) 0.023 (0.020) 13.7 (4.9) 9.8 (8.2) 0.062 (0.030) 0.057 (0.027) 26.5 (11.2) 25.3 (10.8) 0.070 (0.030) 0.033 (0.012) 30.4 (11) 14.7 (4.5)
16 11.1 0.020 0.010 9.7 3.6 0.020 0.030 10 11.1 0.040 0.020 20 9
30.4 20 0.080 0.060 22.2 25 0.110 0.100 44 38.5 0.120 0.050 48 20
5 (p = .041)
ns
ns
ns
ns
2.5 (p = .009)
0.5 (p = .002)
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Fig. 2. Averaged maximum shifts of the center of pressure during the leaning task showing the amplitude of the CoP shifts in four directions as a percentage of the base of support (delimited by the length and width of both feet). The drawing of the feet is not scaled to the values of the graph.
3.2. CoP shifts during arm raising In the forward direction, the maximum shift scaled to the feet length differed significantly between tasks (F(1.34,13.42) = 4.372, p < .047). Pairwise comparisons showed that the effect of tasks was due to the difference between the bilateral condition (mean shift of 11%) and each of the unilateral condition while both unilateral conditions did not differ significantly from each other (for both dominant and non-dominant arm movements the mean was 9%). Adding a weight increased the shift significantly (mean without weight = 7%, mean with weight = 12%, F(1, 10) = 20.527, p < .001). When the maximum shift was scaled to the LOS, the main effect of weight conditions was also significant (F(1,10) = 19.328, p < .001): bilateral arm movements lead to significantly larger relative sway (mean = 66%) than both unilateral movements (mean dominant = 52% and mean non-dominant = 53%) (Fig. 3). The TD children swayed on average significantly a smaller amount of their LOS (mean = 38%) than children with SUCP (mean = 76%, F(1,10) = 13.025, p = .005) (Fig. 4). In the direction of the non-dominant or more-affected leg, the maximum shift scaled to the BOS differed significantly between groups (F(1,10) = 5.687, p = .038) with the shift in the TD group moving over 7% of the total width of the BOS and 18% in the SUCP group. The main effect of group was also significant when the maximum shift was scaled to the LOS (F(1,10) = 5.702, p = .038): the TD children swayed over 27% toward their LOS while the children with SUCP swayed over 155%. No other main or interaction effects were significant.
Fig. 3. Averaged maximum shifts of the center of pressure during the arm raising task showing the amplitude of the CoP shifts during arm movements with and without weights at the wrist, in four directions as a percentage of the base of support (delimited by the length and width of both feet). The drawing of the feet is not scaled to the values of the graph.
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Fig. 4. Averaged maximum shifts of the center of pressure during the arm raising task showing the amplitude of the CoP shifts during arm movements with and without weights at the wrist, in four directions as a percentage of the limits of stability in these directions.
In the backward direction, only the maximum shift scaled to the LOS differed significantly between groups showing that on average TD children swayed over 25% toward their LOS while children with USCP swayed over 68% toward their LOS. In the direction of the dominant or less-affected leg, none of the within and between factors had a significant effect on the maximum shift. 4. Discussion The general aim of this study was to gain more insight in postural control during voluntary upper limb movements in children with USCP. As expected, the results for the leaning task showed that children with USCP had smaller LOS on their more-affected side and in the forward direction compared to the TD children. In contrast, on the less-affected/dominant side, children with USCP were equally able to shift their weight than the TD children. Although the capacity to shift the weight toward the less-affected side in the USCP group was comparable to the control group it did not compensate for the diminished weight shift capacity toward the affected side when leaning forward: maximum leaning forward was also reduced in the USCP group. During arm movements, the forward direction was, as expected, the most sensitive to the variation of amount of disturbance that the movement inflicted upon the body: in both groups, the maximum sway was larger during bilateral movements compared to unilateral movements and also larger when the arms inertia increased (with weight compared to without weight). This is in line with previous studies in children (Hay & Redon, 2001) and in adults (Vernazza-Martin et al., 1999) and shows that children with USCP, as other children, do not maintain their posture within fixed tolerance limits but adapt to the biomechanical consequences of their movements. By doing so, children with USCP may jeopardize their balance more frequently than other individuals while they perform self-paced upper limb movements. The larger relative postural sway during arm movement in this group corroborates this rationale. During rapid arm movements, children with USCP swayed over a larger proportion of their base length and width in the forward direction and on the more-affected side and, as a consequence of their shorter LOS, they swayed closer to their limits in these two directions. While the present results were revealed during rapid movements it is possible that the longer movement time often observed in individuals with USCP (Ricken et al., 2005) might reflect an attempt to reduce the biomechanical perturbation that occur during rapid movements. Remarkably, during arm movements the relative postural sway on the more-affected side scaled to the LOS was larger than the magnitude of the LOS measured during the leaning task. Although the reduced LOS in the forward direction and toward the more-affected side might reflect a lack of motivation to execute the leaning task, the absence of difference with the TD group for the other two directions suggest that the children with USCP did really attempt to lean to what they perceived as their maximum leaning capabilities. Furthermore, the visual targets and visual feedback of the CoP did motivate them to reach the target as far as possible which was corroborated by the experimenters who carried out the experiments. The finding that the sway during rapid arm movement was larger than the sway during leaning indicate that children with USCP might have the strength to cope with large weight shifts toward their more-affected side without losing balance but that they encounter difficulties to voluntarily perform them. Following Forth et al. (2011) we suggest that the shorter LOS in these two directions reflect the self-perceived capabilities and indicate that these margins are not purely biomechanical but are affected by the available sensory information and the ability to integrate it to control movement. Impairment of sensory integration in children with cerebral palsy has been shown previously during stance (Cherng et al., 1999) as during upper limbs movements (Smorenburg et al., 2012) and might account for the discrepancy between the postural sways obtained during voluntarily leaning and during arm movement. When leaning one has to integrate the information from the sole, the muscles, the vestibular system and the visual information about the weight shift in order to perceive the balance limits and rapidly react by sending the appropriate muscle activity to stop the sway. The distance between the maximum voluntarily shift during leaning and the shift in reaction to arm movement might correspond to a disused area where limited explorative
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behavior occur in daily life while strength of the lower limbs would allow more weight shifts toward the more-affected leg. However, the shorter LOS observed on this side might correspond to regions of higher instability as previously described in adults (Duarte & Zatsiorsky, 2002): area for which balance is maintained with increased postural sway and consequently higher physiological cost. Due to limited time the children had to maintain the leaning positions in each direction (about 1 s) the present results did not allow to relate the characteristics of postural sway toward the LOS during voluntary leaning with the sway during the arm movements. Nevertheless, we suggest that the presence of asymmetric LOS is an indicator of decreased postural control toward the affected side and that postural sway that comes close to these boundaries threatens balance. Encouraging results obtained after a period of training with weight-shifting tasks showed that LOS can be trained in children with USCP (Ledebt et al., 2005) and in patients with other conditions that lead to asymmetrical postural sway (Barnett et al., 2013). Further research is required to assess whether the increase of the LOS may in turn have consequence for the maintenance of stability, the preparatory postural adjustments and execution of suprapostural tasks. As shown in healthy adults, stability limits and the way individuals are approaching them can affect motor learning (Manista & Ahmed, 2012) and gait symmetry (Hendrickson et al., 2013) and may therefore afford new perspectives to investigate and train balance and locomotion. The present results are in line with previous results obtained in individuals with other type of balance problems (Forth et al., 2011; Slobounov et al., 1998). Although the number of participants is small, the results shows that spatial measures of the stability margins are at least equally, or even more sensitive to the postural imbalance than the traditional summary measures of the center of pressure. The LOS might also be a relevant aspect to investigate the impact of ankle–foot ortheses on standing balance. Furthermore, enlarging the LOS by active exploration of weight-shifts should increase the area of permissible sway and thus increase the functional base of support. More specifically, enlarging the LOS toward the affected side and in the forward direction is expected to reduce the impact of supra-postural tasks involving the upper-limbs in front of the patients, on the maintenance of stability. Training toward these limits include the dual aim of increasing the awareness of one’s possibilities (the self-perceived limits of stability) as well as improving the neuro-muscular coordination to control the weight-shifts toward the more-affected limb. Acknowledgements The authors would like to thank the children and their parents for their voluntary participation in the study and Aurelie Fortune for her assistance during the data collection. References Barnett, C. T., Vanicek, N., & Polman, R. C. (2013). Postural responses during volitional and perturbed dynamic balance tasks in new lower limb amputees: A longitudinal study. Gait & Posture, 37, 319–325. Bouisset, S., & Zattara, M. (1987). Biomechanical study of the programming of anticipatory postural adjustments associated with voluntary movement. Journal of Biomechanics, 20, 735–742. Cherng, R. J., Su, F. C., Chen, J. J., & Kuan, T. S. (1999). Performance of static standing balance in children with spastic diplegic cerebral palsy under altered sensory environments. American Journal of Physical Medicine & Rehabilitation, 78, 336–343. Donker, S. F., Ledebt, A., Roerdink, M., Savelsbergh, G. J. P., & Beek, P. J. (2008). Children with cerebral palsy exhibit greater and more regular postural sway than typically developing children. Experimental Brain Research, 184, 363–370. Duarte, M., & Zatsiorsky, V. M. (2002). Effects of body lean and visual information on the equilibrium maintenance during stance. Experimental Brain Research, 146, 60–69. Forth, K. E., Fiedler, M. J., & Paloski, W. H. (2011). Estimating functional stability boundaries for bipedal stance. Gait & Posture, 33, 715–717. Hay, L., & Redon, C. (2001). Development of postural adaptation to arm raising. Experimental Brain Research, 139, 224–232. Hendrickson, J., Patterson, K. K., Inness, E. L., McIlroy, W. E., & Mansfield, A. (2013). Relationship between asymmetry of quiet standing balance control and walking post-stroke. Gait & Posture. Ledebt, A., Becher, J., Kapper, J., Rozendaal, R. M., Bakker, R., Leenders, I. C., & Savelsbergh, G. J. P. (2005). Balance training with visual feedback in children with hemiplegic cerebral palsy: Effect on stance and gait. Motor Control, 9, 459–468. Manista, G. C., & Ahmed, A. A. (2012). Stability limits modulate whole-body motor learning. Journal of Neurophysiology, 107, 1952–1961. Ricken, A. X., Bennett, S. J., & Savelsbergh, G. J. P. (2005). Coordination of reaching in children with spastic hemiparetic cerebral palsy under different task demands. Motor Control, 9, 357–371. Roncesvalles, M. N. C., Woollacott, M. H., & Jensen, J. L. (2000). The development of compensatory stepping skills in children. Journal of Motor Behavior, 32, 100–111. Slobounov, S. M., Moss, S. A., Slobounova, E. S., & Newell, K. M. (1998). Aging and time to instability in posture. Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 53, B71–B78. Smorenburg, A. R. P., Ledebt, A., Deconinck, F. J. A., & Savelsbergh, G. J. P. (2012). Deficits in upper limb position sense of children with spastic hemiparetic cerebral palsy are distance-dependent. Research in Developmental Disabilities, 33, 971–981. Stackhouse, C., Shewokis, P. A., Pierce, S. R., Smith, B., McCarthy, J., & Tucker, C. (2006). Gait initiation in children with cerebral palsy. Gait & Posture. Tomita, H., Fukaya, Y., Honma, S., Ueda, T., Yamamoto, Y., & Shionoya, K. (2010). Anticipatory postural muscle activity associated with bilateral arm flexion while standing in individuals with spastic diplegic cerebral palsy: A pilot study. Neuroscience Letters, 479, 166–170. Vernazza-Martin, S., Martin, N., Cincera, M., Pedotti, A., & Massion, J. (1999). Arm raising in humans under loaded vs. unloaded and bipedal vs. unipedal conditions. Brain Research, 846, 12–22. Woollacott, M., Shumway-Cook, A., Hutchinson, S., Ciol, M., Price, R., & Kartin, D. (2005). Effect of balance training on muscle activity used in recovery of stability in children with cerebral palsy: A pilot study. Developmental Medicine & Child Neurology, 47, 455–461.
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Postural adaptation during arm raising in children with and without unilateral cerebral palsy Annick Ledebt *, Geert J.P. Savelsbergh Research Institute MOVE, Faculty of Human Movement Sciences, VU University Amsterdam, Van Der Boechorststraat 9, Amsterdam 1081 BT, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 October 2013 Received in revised form 10 February 2014 Accepted 14 February 2014 Available online 23 March 2014
Postural sway during arm movements were related to the size of the base of support (BOS) and the limits of stability (LOS) of children with unilateral cerebral palsy (USCP) and typically developing (TD) children. For half of the trials the mechanical disturbance due to the rapid arm movement was increased by attaching small weights at the wrists. The participants stood with both feet on a large force plate, which recorded the displacements of the center of pressure (CoP). The results showed that in the children with USCP the LOS forward and toward the non-dominant (more-affected) side were smaller than in the TD children whereas the LOS backward and toward the dominant (less-affected) side did not differ between the two groups. When rapidly moving the arms the children with USCP swayed over a larger portion of their base of support in the forward direction and toward their more-affected side. In addition, the maximal sway toward the more-affected side during arm movement exceeded the LOS while balance was maintained. These effects increased when the movements were performed with the weights at the wrists. These results show that an area of permissible sway, which was not spontaneously explored during the leaning task, was required to maintain balance during the supra-postural task. Training to enlarge the LOS that includes weight shifts toward the more-affected side might reduce the area of the BOS that is self-perceived as less secure. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Congenital hemiparesis Balance Postural adjustments Center of pressure Limits of stability Base of support
1. Introduction Poor postural control has been suggested to be one of the underlying factors to the frequent abnormal motor development in children with cerebral palsy (Roncesvalles et al., 2000). Functional level of children with cerebral palsy is ranged from independent walking with minimal walking aids (e.g., ankle–foot ortheses) to wheelchair bounded mobility. Although children with unilateral cerebral palsy (UCP) are usually high functioning and able to stand and walk independently they still encounter problems during stance when rapid weight shifts are required in preparation (Stackhouse et al., 2006) or in reaction to a perturbation (Woollacott et al., 2005). During quiet standing, children with UCP exhibit greater and more regular sway than typically developing children (Donker et al., 2008). These results have been viewed as the dynamical signature of poor postural control in children with UCP during quiet standing. Quiet standing is rarely maintained for its own sake but instead facilitates the performance of daily suprapostural tasks like visual tasks and voluntary movements of the upper limbs. Many studies have shown that in adults and typically developing children postural
* Corresponding author. Tel.: +31 20 5988462; fax: +31 20 5988529. E-mail address: [email protected] (A. Ledebt). http://dx.doi.org/10.1016/j.ridd.2014.02.007 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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adjustments contribute to the preparation and execution of arm movements. As the movements of one or two arms contribute to the displacement of the center of mass, the position of the center of pressure (COP) has to be adjusted accordingly in order to maintain equilibrium (Bouisset & Zattara, 1987). The postural adjustments counteract the destabilizing effect of the arm movements which increases when additional constraints are involved such as extra load at the arm (Hay & Redon, 2001). The potentially destabilizing effect of such arm movements on bipedal stance is also related to the size of the area of functional postural sway. The borders of this area, the limits of stability (LOS), correspond to the region of transition from bipedal stance to stepping (Duarte & Zatsiorsky, 2002). The LOS area is commonly smaller than the base of support as defined by the geometry of the feet (BOS) and is usually evaluated for different leaning orientations (Duarte and Zatsiorsky, 2002; Forth et al., 2011). The results in adults showed that spatial variability of the postural sway increased toward the LOS when leaning increased while both feet maintained full contact with the ground. In children with cerebral palsy only preparatory adjustments to self-paced arm movement have been reported (Tomita et al., 2010) while it is still unclear how postural adjustments unfold during arm movements as a function of the BOS and the LOS. The aim of the present study was to analyze the postural adaptation during unilateral and bilateral rapid arm movement and to relate these postural shifts to the size of the base of support (BOS) and to the limits of support (LOS). Rapid movements and increased inertia (small loads at the wrists) were used to investigate the postural reactions when perturbation forces due to movements are maximized. Although the most relevant direction to analyze with respect to this task was the forward direction (Bouisset & Zattara, 1987), backward sway and sway toward the dominant and non-dominant side might reveal asymmetrical behavior in individuals with USCP. Therefore the study analyzed the global outcome of the adaptation as reflected in the shifts of the COP in relation to functional limits of standing posture defined as the base of support and the limits of stability. We expected that individuals with USCP show smaller limits of stability than TD children specifically along the medio-lateral axis in relation to the weakness of their more-affected leg. As a consequence it was expected that during arm movements the maximum postural sway would be closer to the LOS in the children with CP than in the TD group. This effect was expected to be enhanced in higher disturbing arm movements, i.e. during bilateral movements and when a small weight was added at the wrists. 2. Methods 2.1. Participants Six children with congenital hemiplegia and six typically developing children without known motor impairments participated in the experiment (see Table 1). All children with USCP could stand and walk independently in accordance with the highest functional mobility level of the Gross Motor Functioning Classification System (GMFCS level I). Their gross motor functioning was further documented according to the ability to jump (starting and ending on both feet) and to hop (small jump starting and ending on the same foot) on one and the other side (see Table 1). All children were able to understand and follow the instructions and to execute the arm raising task without restriction or pain. One child with USCP was using an ankle–foot orthesis on a daily basis. All children and their parents gave their informed consent prior to participation. The experiment was carried out in compliance with the Helsinki Declaration and was endorsed by the University Medical Centre Amsterdam. 2.2. Procedure and apparatus Participants stood upright on a 1 m 1 m custom-made strain gauge force plate (sampling rate 100 Hz). Their feet were placed parallel to the anterior–posterior axis of the force plate and the distance between the feet corresponded to pelvis width. Children wore their own shoes, including ankle–foot ortheses when necessary (only child OT) in order to correspond Table 1 Participants’ characteristics. Participant
Group
Height (cm)
Gender
Age (years)
Non-dominant/ affected side
Jump (two legs)
Hop on non-dom. leg
Hop on dom. leg
ES NC AE OT NK NJ EM ER OT TB ND YG
TD TD TD TD TD TD CP CP CP CP CP CP
1140 1150 1360 1410 1440 1430 1130 1140 1160 1340 1440 1510
F M F M F M M M M F M F
5 6 7 9 9 11 5 6 6 8 9 11
L L L L L L R R La R L R
Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes
Yes Yes Yes Yes Yes Yes No No No No No No
Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes Yes
a
Ankle–foot orthosis on affected side.
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to what they experienced in daily life. The positioning of the feet on the floor was drawn on a paper fixed to the force plate. This positioning was then maintained for the different tasks, which included voluntary leaning and arm raising while standing. The procedure followed during the leaning trials already presented elsewhere (Ledebt et al., 2005) and used a visual feedback of the COP displayed on a screen in front of the participant. A dot corresponding to the COP was visible and was moving online with the weight shifts of the child. The child was instructed to slowly move the dot in order to reach visual targets while keeping both feet completely on the ground and encouraged to use an ankle strategy (‘‘move as a block’’) rather than a hip or a mixed strategy. The targets appeared on the screen along the antero-posterior and medio-lateral axes at increasing distances from the neutral position of the COP. This way the child was motivated to lean as far as possible forward, backward, on the dominant (non-affected) leg and on the non-dominant (affected) leg. Time was given to experience the effect of own movements on the screen before the recordings were made and lasted not longer than a few minutes. The amplitude of the largest sway in each of the four directions was measured from the force plate data. For the arm raising task the children had to quickly raise one or both arms toward light emitting diodes (LED) placed in front of the shoulders after the LED turned on (right or left arm moving after respectively switching on the right or left LED and both arms when both LEDs switched on). The end position of the arms was horizontal and had to be maintained a few seconds (when LED switched off). A small uniaxial accelerometer (ICSensors 3145-002, piezoresistive sensor, linearity range: 2 g) was attached at each wrist in order to detect the beginning and the end of the arm movement. The signal of the accelerometer contains a component of the gravitational acceleration and a component of the inertial acceleration: in the absence of movement the accelerometer signal yielded inclination information while during movement this information was combined with acceleration information. During a few trying out trials it was checked that the child was able to move rapidly at least within a second between start and end position. Six conditions were applied corresponding to a fully crossed design including two factors: three arm conditions (unilateral dominant, unilateral non-dominant and bilateral) and two weight conditions (with and without addition weight at the wrists). The weight corresponded to 2% of participant’s weight at each wrist. A total of 30 arm raising trials were presented in two separate blocks, one block with and one block without weights. The order of these two blocks was counterbalanced across participants. Within each block, the 15 trials (3 arm conditions and 5 trials per conditions) were randomly presented. 2.3. Data analysis Prior to all analyses, the mean was subtracted from medio-lateral and anteroposterior CoP trajectories. The resulting time series were then filtered (second-order low-pass Butterworth filter, cut-off frequency 12.5 Hz). The maximum amplitude of the CoP trajectories along both axes was calculated for the leaning and the arm raising trials. During the leaning trials the maximum forward, backward, toward the paretic/non-dominant and toward the non-paretic/dominant side displacements were considered when maintained at least during one second. During the arm raising trials the maximum displacement in the same four directions were considered when occurring during the time the arm was moving. The beginning and the end of the arm movement were indicated by the wrist accelerometer signals (see Fig. 1). The baseline level of CoP position was calculated as the mean position of the CoP between 400 ms and 200 ms before movement onset. In addition to the absolute values of the maximum amplitudes two indexes were computed for the leaning trials and the arm raising trials respectively. As a large range of feet length in both groups of children was expected (due to the large age ranges), the maximum sway were first scaled to with respect to the BOS. The forward and backward LOS were scaled to the subject’s base of support (BOS) length as measured on the paper fixed on the force plate whereas the LOS toward the affected/non-dominant and toward the non-affected/dominant side were scaled to the width of the base of support (LOS/ BOS ratio). The width of the BOS was calculate as the average of the largest distance (usually at toes level) and the shortest distance (usually located at heel level) of the outer limits of the BOS. An identical procedure was used to scale the maximum shifts measured during arm movement to the BOS (expressed in percentage). Maximum shifts during arm movement were also scaled to the corresponding LOS for each of the four directions (expressed in percentage). The differences between children with CP and the TD children for BOS length and width and for the absolute and relative LOS (in all four directions) were analyzed by a Mann–Whitney U test. For each sway direction, the absolute and relative maximum shifts during arm raising were analyzed by a three-way 2 3 2 (group arm weight) analysis of variance, with repeated measures on the last two factors. Data are expressed as mean SD and statistical significance was accepted at p < 0.05. A Greenhouse–Geisser correction was applied when the underlying assumption of homogeneity was violated. 3. Results 3.1. CoP shifts during voluntary leaning Although on the average the base length and width did not differ between the two groups, base length maximum values indicated that the variability in the TD group was larger than in the CP group (Table 2). The absolute and relative LOS in the forward and non-dominant/affected direction was significantly smaller in the CP group than in the TD group and failed to be significant for the two other directions (Fig. 2).
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Fig. 1. Typical postural sway during the execution of a unilateral arm movement with the dominant arm of this participant (right arm). On the left, from top to bottom: displacement of the center of pressure along the sagittal axis (CoPx) and the medio-lateral axis (CoPy) and tangential acceleration recorded at the wrist (Acc.). Time zero represents the onset of arm movement indicated by an increase of acceleration followed by a decrease before arm stabilizes in the new position. The maximum displacement of the CoP was measured between the start and the end of the movement in four directions backward (CoPmax back), forward (CoPmax forw), on the dominant side (CoPmax dom) and the non-dominant side (CoPmax non-dom). The vertical bar on the bottom line indicates the moment the visual signal for the start of the movement turned on (LED). On the right: the same antero-posterior and medio-lateral displacements of the CoP are represented without the time line.
Table 2 Base of support and limits of stability. Mean (SD) Base length (m) TD CP Base width (m) TD CP LOS Forward (m) TD CP LOS Forward/BOS (%) TD CP LOS Backward (m) TD CP LOS Backward/BOS (%) TD CP LOS Dominant (m) TD CP LOS Dom/BOS (%) TD CP LOS Non-Dominant (m) TD CP LOS Non-Dom/BOS (%) TD CP
Min
Max
Mann–Whitney U
0.255 (0.665) 0.243 (0.326)
0.19 0.20
0.36 0.28
ns
0.226 (0.186) 0.225 (0.32)
0.20 0.20
0.25 0.27
ns
0.055 (0.014) 0.037 (0.008)
0.040 0.030
0.070 0.050
4.5 (p = .026)
24.3 (5.7) 16.4 (3.4) 0.036 (0.022) 0.023 (0.020) 13.7 (4.9) 9.8 (8.2) 0.062 (0.030) 0.057 (0.027) 26.5 (11.2) 25.3 (10.8) 0.070 (0.030) 0.033 (0.012) 30.4 (11) 14.7 (4.5)
16 11.1 0.020 0.010 9.7 3.6 0.020 0.030 10 11.1 0.040 0.020 20 9
30.4 20 0.080 0.060 22.2 25 0.110 0.100 44 38.5 0.120 0.050 48 20
5 (p = .041)
ns
ns
ns
ns
2.5 (p = .009)
0.5 (p = .002)
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Fig. 2. Averaged maximum shifts of the center of pressure during the leaning task showing the amplitude of the CoP shifts in four directions as a percentage of the base of support (delimited by the length and width of both feet). The drawing of the feet is not scaled to the values of the graph.
3.2. CoP shifts during arm raising In the forward direction, the maximum shift scaled to the feet length differed significantly between tasks (F(1.34,13.42) = 4.372, p < .047). Pairwise comparisons showed that the effect of tasks was due to the difference between the bilateral condition (mean shift of 11%) and each of the unilateral condition while both unilateral conditions did not differ significantly from each other (for both dominant and non-dominant arm movements the mean was 9%). Adding a weight increased the shift significantly (mean without weight = 7%, mean with weight = 12%, F(1, 10) = 20.527, p < .001). When the maximum shift was scaled to the LOS, the main effect of weight conditions was also significant (F(1,10) = 19.328, p < .001): bilateral arm movements lead to significantly larger relative sway (mean = 66%) than both unilateral movements (mean dominant = 52% and mean non-dominant = 53%) (Fig. 3). The TD children swayed on average significantly a smaller amount of their LOS (mean = 38%) than children with SUCP (mean = 76%, F(1,10) = 13.025, p = .005) (Fig. 4). In the direction of the non-dominant or more-affected leg, the maximum shift scaled to the BOS differed significantly between groups (F(1,10) = 5.687, p = .038) with the shift in the TD group moving over 7% of the total width of the BOS and 18% in the SUCP group. The main effect of group was also significant when the maximum shift was scaled to the LOS (F(1,10) = 5.702, p = .038): the TD children swayed over 27% toward their LOS while the children with SUCP swayed over 155%. No other main or interaction effects were significant.
Fig. 3. Averaged maximum shifts of the center of pressure during the arm raising task showing the amplitude of the CoP shifts during arm movements with and without weights at the wrist, in four directions as a percentage of the base of support (delimited by the length and width of both feet). The drawing of the feet is not scaled to the values of the graph.
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Fig. 4. Averaged maximum shifts of the center of pressure during the arm raising task showing the amplitude of the CoP shifts during arm movements with and without weights at the wrist, in four directions as a percentage of the limits of stability in these directions.
In the backward direction, only the maximum shift scaled to the LOS differed significantly between groups showing that on average TD children swayed over 25% toward their LOS while children with USCP swayed over 68% toward their LOS. In the direction of the dominant or less-affected leg, none of the within and between factors had a significant effect on the maximum shift. 4. Discussion The general aim of this study was to gain more insight in postural control during voluntary upper limb movements in children with USCP. As expected, the results for the leaning task showed that children with USCP had smaller LOS on their more-affected side and in the forward direction compared to the TD children. In contrast, on the less-affected/dominant side, children with USCP were equally able to shift their weight than the TD children. Although the capacity to shift the weight toward the less-affected side in the USCP group was comparable to the control group it did not compensate for the diminished weight shift capacity toward the affected side when leaning forward: maximum leaning forward was also reduced in the USCP group. During arm movements, the forward direction was, as expected, the most sensitive to the variation of amount of disturbance that the movement inflicted upon the body: in both groups, the maximum sway was larger during bilateral movements compared to unilateral movements and also larger when the arms inertia increased (with weight compared to without weight). This is in line with previous studies in children (Hay & Redon, 2001) and in adults (Vernazza-Martin et al., 1999) and shows that children with USCP, as other children, do not maintain their posture within fixed tolerance limits but adapt to the biomechanical consequences of their movements. By doing so, children with USCP may jeopardize their balance more frequently than other individuals while they perform self-paced upper limb movements. The larger relative postural sway during arm movement in this group corroborates this rationale. During rapid arm movements, children with USCP swayed over a larger proportion of their base length and width in the forward direction and on the more-affected side and, as a consequence of their shorter LOS, they swayed closer to their limits in these two directions. While the present results were revealed during rapid movements it is possible that the longer movement time often observed in individuals with USCP (Ricken et al., 2005) might reflect an attempt to reduce the biomechanical perturbation that occur during rapid movements. Remarkably, during arm movements the relative postural sway on the more-affected side scaled to the LOS was larger than the magnitude of the LOS measured during the leaning task. Although the reduced LOS in the forward direction and toward the more-affected side might reflect a lack of motivation to execute the leaning task, the absence of difference with the TD group for the other two directions suggest that the children with USCP did really attempt to lean to what they perceived as their maximum leaning capabilities. Furthermore, the visual targets and visual feedback of the CoP did motivate them to reach the target as far as possible which was corroborated by the experimenters who carried out the experiments. The finding that the sway during rapid arm movement was larger than the sway during leaning indicate that children with USCP might have the strength to cope with large weight shifts toward their more-affected side without losing balance but that they encounter difficulties to voluntarily perform them. Following Forth et al. (2011) we suggest that the shorter LOS in these two directions reflect the self-perceived capabilities and indicate that these margins are not purely biomechanical but are affected by the available sensory information and the ability to integrate it to control movement. Impairment of sensory integration in children with cerebral palsy has been shown previously during stance (Cherng et al., 1999) as during upper limbs movements (Smorenburg et al., 2012) and might account for the discrepancy between the postural sways obtained during voluntarily leaning and during arm movement. When leaning one has to integrate the information from the sole, the muscles, the vestibular system and the visual information about the weight shift in order to perceive the balance limits and rapidly react by sending the appropriate muscle activity to stop the sway. The distance between the maximum voluntarily shift during leaning and the shift in reaction to arm movement might correspond to a disused area where limited explorative
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behavior occur in daily life while strength of the lower limbs would allow more weight shifts toward the more-affected leg. However, the shorter LOS observed on this side might correspond to regions of higher instability as previously described in adults (Duarte & Zatsiorsky, 2002): area for which balance is maintained with increased postural sway and consequently higher physiological cost. Due to limited time the children had to maintain the leaning positions in each direction (about 1 s) the present results did not allow to relate the characteristics of postural sway toward the LOS during voluntary leaning with the sway during the arm movements. Nevertheless, we suggest that the presence of asymmetric LOS is an indicator of decreased postural control toward the affected side and that postural sway that comes close to these boundaries threatens balance. Encouraging results obtained after a period of training with weight-shifting tasks showed that LOS can be trained in children with USCP (Ledebt et al., 2005) and in patients with other conditions that lead to asymmetrical postural sway (Barnett et al., 2013). Further research is required to assess whether the increase of the LOS may in turn have consequence for the maintenance of stability, the preparatory postural adjustments and execution of suprapostural tasks. As shown in healthy adults, stability limits and the way individuals are approaching them can affect motor learning (Manista & Ahmed, 2012) and gait symmetry (Hendrickson et al., 2013) and may therefore afford new perspectives to investigate and train balance and locomotion. The present results are in line with previous results obtained in individuals with other type of balance problems (Forth et al., 2011; Slobounov et al., 1998). Although the number of participants is small, the results shows that spatial measures of the stability margins are at least equally, or even more sensitive to the postural imbalance than the traditional summary measures of the center of pressure. The LOS might also be a relevant aspect to investigate the impact of ankle–foot ortheses on standing balance. Furthermore, enlarging the LOS by active exploration of weight-shifts should increase the area of permissible sway and thus increase the functional base of support. More specifically, enlarging the LOS toward the affected side and in the forward direction is expected to reduce the impact of supra-postural tasks involving the upper-limbs in front of the patients, on the maintenance of stability. Training toward these limits include the dual aim of increasing the awareness of one’s possibilities (the self-perceived limits of stability) as well as improving the neuro-muscular coordination to control the weight-shifts toward the more-affected limb. Acknowledgements The authors would like to thank the children and their parents for their voluntary participation in the study and Aurelie Fortune for her assistance during the data collection. References Barnett, C. T., Vanicek, N., & Polman, R. C. (2013). Postural responses during volitional and perturbed dynamic balance tasks in new lower limb amputees: A longitudinal study. Gait & Posture, 37, 319–325. Bouisset, S., & Zattara, M. (1987). Biomechanical study of the programming of anticipatory postural adjustments associated with voluntary movement. Journal of Biomechanics, 20, 735–742. Cherng, R. J., Su, F. C., Chen, J. J., & Kuan, T. S. (1999). 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