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Balance problems during obstacle crossing in children with Developmental Coordination Disorder
Gait & Posture 32 (2010) 327–331
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Balance problems during obstacle crossing in children with Developmental Coordination Disorder F.J.A. Deconinck a,c,*, G.J.P. Savelsbergh a,b, D. De Clercq c, M. Lenoir c a
Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan University, UK Research Institute MOVE, VU University Amsterdam, The Netherlands c Department of Movement and Sports Sciences, Ghent University, Belgium b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 19 August 2009 Received in revised form 27 May 2010 Accepted 29 May 2010
The present study investigated the visuomotor and balance limitations during obstacle crossing in typically developing (TD) children and those with Developmental Coordination Disorder (DCD) (7–9 years old; N = 12 per group). Spatiotemporal gait parameters as well as range and velocity of the centre of mass (COM) were determined in three conditions: overground walking at a self-selected speed, crossing a low obstacle and crossing a high obstacle (5% or 30% of the leg length, respectively). Both groups walked more slowly during obstacle crossing than walking over level ground. In addition, both groups exhibited a significant decrease in the spatial variability of their foot placements as they approached the obstacle, which was then negotiated with a similar strategy. There were no differences in approach distance, length of lead and trail step, or lead and trail foot elevation. Compared to walking over level ground, obstacle crossing led to a longer swing phase of the lead and trail foot and increased maximal mediolateral COM velocity. In children with DCD, however, medio-lateral COM velocity was higher and accompanied by significantly greater medio-lateral COM amplitude. In conclusion, the results indicate that while TD-children and those with DCD exhibit satisfactory anticipatory control and adequate visual guidance, the latter group have a reduced ability to control the momentum of the COM when crossing obstacles that impose increased balance demands. Crown Copyright ß 2010 Published by Elsevier B.V. All rights reserved.
Keywords: Developmental Coordination Disorder (DCD) Gait Balance Anticipation Obstacle crossing Perceptuo-motor control
1. Introduction Children with Developmental Coordination Disorder (DCD) experience difficulties acquiring and performing motor skills, which then inhibits participation in physical activities and puts them at risk of long-term health and psycho-social problems [1,2]. DCD is not caused by a known neurological or physical pathology and has a prevalence rate of about 6% in 5–11-year-old children [1]. The clumsy motor behaviour associated with DCD is thought to originate from perceptual deficits [3] and problems involving feedback and/or feedforward control mechanisms [4]. However, it remains unclear if, and how, these deficits in motor control contribute to the completion of daily activities. In this study, we compare obstacle crossing behaviour in a group of children with DCD and a group of typically developing children. Obstacle crossing is examined because it demands precise postural and
* Corresponding author at: Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan University, John Dalton Building, Oxford Road, Manchester M1 5GD, United Kingdom. Tel.: +44 0161 247 5532; fax: +44 0161 247 6375. E-mail address: [email protected] (F.J.A. Deconinck).
balance control using perceptually driven anticipatory adjustments. (e.g. [5,6]). In this respect, a detailed examination of the gait pattern and the motion of the centre of mass during obstacle crossing can elucidate to what extent these perceptuo-motor systems limit ambulation in children with DCD. Research into obstacle crossing in the elderly or in individuals following traumatic brain injury highlights the particular role of balance control during this task. It has been shown that imbalance leads to an increase in amplitude and velocity of medio-lateral centre of mass (COM) motion and a suppression of gait adaptations that are inherent to obstacle crossing, but may render the body unstable (e.g. increased separation of COM, and centre of pressure, COP) [7,8]. In combination, excessive COM motion and failure to make the required gait adaptations could lead to an increased incidence of falling. To compensate, participants with low balance confidence exhibit a larger safety margin for foot clearance, wider base of support, slower velocity during the approach, and smaller step length [9–12]. Problems with postural control have been suggested to explain the a-typical gait pattern of children with DCD [13], which is characterised by shorter steps, greater trunk inclination, decreased ankle flexion and more variable thigh and shank movement than typically developing (TD) children [14,15]. Such behavioural adaptations when walking in children with DCD have been shown
0966-6362/$ – see front matter . Crown Copyright ß 2010 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2010.05.018
F.J.A. Deconinck et al. / Gait & Posture 32 (2010) 327–331
328 Table 1 Information on the participants of both groups.
n Age Gender Length Body weight Physical activity MABC percentile
Children with DCD
Children without DCD
12 7.8 0.5 years 10 boys/2 girls 126.8 4.9 cm 25.6 4.4 kg 4.3 1.8 h/week 5.0 3.8
12 7.7 0.6 years 10 boys/2 girls 127.5 0.6 cm 25.6 3.4 kg 4.8 1.8 h/week 78.3 17.3
Note: MABC is Movement Assessment Battery for Children.
to demand a greater reliance on visual information [16,17]. However, given the reported visuomotor difficulties [3] and decreased visual sensitivity [18] in children with DCD, it is possible that the increased demand for precise visual information on distance and height of an obstacle [19–21] could limit the performance of a stable and adaptive gait. This may be manifested in poor anticipatory planning during the approach (with increased spatial variability and/or inappropriate foot positioning) and more unsuccessful crossings. In this way, children with DCD could be particularly vulnerable to the balance constraints imposed when confronting an obstacle, possibly leading to more cautious behaviour and excessive COM motion in medio-lateral direction during the crossing phase. In summary, the aim of this study was to examine visuomotor and balance limitations during obstacle crossing in typically developing (TD) children and those with Developmental Coordination Disorder (DCD). Given the documented difficulties with balance and visual perception, children with DCD were expected to demonstrate more signs of instability and less accurate foot positioning leading to more unsuccessful crossings. 2. Methods 2.1. Participants 12 children with DCD (age 7–9) and 12 TD-children participated in the study (see Table 1 for details). The children with DCD were free from co-morbid neurodevelopmental disorders as diagnosed by a neuro-paeditrician after a multidisciplinary assessment of their neurological health, motor skills, psychological behaviour and intellectual capacities. Their motor competence was tested with the Movement Assessment Battery for Children, which is a norm-referenced basic motor abilities assessment tool containing fine motor, ball handling, and balance tasks [22], and was indicated to be well below average (all children < 15th percentile, 7 children < 5th percentile). The TD-children with normal motor proficiency were matched on gender, age, body length, weight and nature and degree of physical activity. Details of the matching procedure are reported elsewhere [13]. The experimental protocol was in accordance with the guidelines of the Declaration of Helsinki and approved by the Ethical Committee of the Ghent University Hospital (ref.: 2002/041). 2.2. Materials and procedure Children were instructed to walk along a 9.6 m walkway, which was surrounded by eight ProReflex infrared cameras operating at a sampling frequency 240 Hz
[(Fig._1)TD$IG]
(Qualisys, Gothenburg, Sweden; Fig. 1). The experiment consisted of three walking conditions: (1) level walking without an obstacle (0%), (2) crossing a low obstacle of height equal to 5% of the leg length (3.5 cm on average), and (3) crossing a high obstacle of height equal to 30% of the leg length (16.6 cm). The obstacle was a rod, loosely attached to two stands at either side of the walkway. The obstacle was placed 4.5 m from the starting position throughout all trials. Reflective markers were attached bilaterally to 16 anatomical landmarks: nail of big toe, caput of the fifth metatarsal, lateral malleolus, lateral epicondyle (femur), anterior superior iliac spine, acromion, lateral epicondyle (humerus), and styloid process (ulna). Additional markers were attached to the process of C7 and L5. Prior to the experiment a demonstration of each walking condition was given. Children were then instructed to walk barefoot at a self-selected, comfortable, and steady pace towards a giant puzzle located at the end of the walkway (used as a diversionary task to motivate children). In the obstacle conditions, children were asked to step over the rod without hesitation and while continuing to walk in a straight line. No directions were given regarding which leg should act as the lead leg and hence clear the obstacle first. Each walking condition was practiced twice before data collection commenced in order to ensure that the child understood and was able to perform the task. Five trials were recorded in each of the three walking conditions, with level walking and obstacle crossing completed in separate blocks. The 10 trials involving obstacle crossing were received in random order. 2.3. Dependent variables and analysis For each of the 15 trials, foot contact (FC) and foot off (FO) were determined based upon validated algorithms described in [23]. The three-dimensional position data were then smoothed with a Butterworth low-pass filter (cut-off: 10 Hz). Subsequent analysis was focused on the crossing stride, which included movement from final FC before the obstacle to the next FC of the same foot. The crossing stride thus comprised lead and trail limb clearance. For each crossing stride we extracted stride velocity, stride time and stride length. In addition, duration, length and width of the lead and trail step, as well as total double support time, were considered. Finally, approach and clearance distance (i.e., horizontal distance between obstacle and ankle of trail and lead foot, respectively), and clearance height for both limbs (i.e., vertical distance between obstacle and toe) were calculated. In order to evaluate consistency of anticipatory adjustments during the approach, withinsubject inter-trial variability (SD) of the obstacle-toe distance for the final threefoot contacts (step 3, 2, and 1) was calculated over five trials. For level walking, measures were based on one stride (starting with foot contact of the right foot) per trial halfway the walkway. Maximal vertical toe height during swing was taken as an alternative to obstacle clearance height. A 15-segment model based on Jensen’s developmental regression equations for relative segment masses and centres [24] was used to calculate the position of the centre of mass (COM) Medio-lateral range of motion (ROM) and maximal velocity of the COM were calculated as measures of dynamic balance during the crossing stride. To examine the effect of obstacle height, spatiotemporal and COM variables were submitted to separate two-way repeated measures ANOVA; Obstacle height [0%, 5%, 30%] Group [DCD, TD]. The exception was foot placement variability and approach distance, which were submitted to separate three-way repeated measures ANOVA; Step [ 3, 2, 1] Obstacle height [0%, 5%, 30%] Group [DCD, TD]. Greenhouse–Geisser adjustments were applied in the event that the sphericity assumption was violated. Main and interaction effects were further examined with Tukey’s HSD post hoc tests, and alpha level was set at p < .05.
3. Results There was no difference in success rate between the groups (DCD: 93.3% or 112/120 trials; TD: 96.6% or 116/120 trials). In the event of an error, this was caused by trail foot contact with the obstacle and was due to impulsiveness rather than incompetence.
Fig. 1. Schematic illustration of the task with indication of dependent variables approach and clearance distance.
F.J.A. Deconinck et al. / Gait & Posture 32 (2010) 327–331
329
Table 2 Means, standard deviations and statistical outcome of the repeated measures ANOVA for the spatiotemporal parameters of the crossing stride. Condition
TD-children
Children with DCD
Group
Obstacle
Group Obstacle
Stride velocity (m/s)
0% 5% 30%
1.317 0.125 1.094 0.108 0.937 .0179
1.292 0.954 0.990 0.159 0.889 0.132
F(1,22) = 1.838 p = .180 h2 = .080
F(2,44) = 55.022 p = .001 h2 = .714
F(2,44) = 1.523 p = .230 h2 = .068
Stride length (m)
0% 5% 30%
1.100 0.087 1.119 0.118 1.098 0.130
1.072 0.093 1.071 0.108 1.023 0.136
F(1,22) = 1.393 p = .251 h2 = .062
F(2,44) = 1.833 p = .173 h2 = .080
F(2,44) = 0.782 p = .464 h2 = .036
Lead step length (m)
0% 5% 30%
0.558 0.054 0.605 0.056 0.627 0.066
0.541 0.050 0.608 0.065 0.641 0.093
F(1,22) = 0.775 p = .389 h2 = .036
F(2,44) = 11.990 p = 0.001 h2 = .363
F(2,44) = 1.748 p = .187 h2 = .077
Trail step length (m)
0% 5% 30%
0.542 0.054 0.513 0.069 0.470 0.055
0.531 0.045 0.463 0.066 0.441 0.055
F(1,22) = 1.729 p = .203 h2 = .076
F(2,44) = 19.869 p = 0.001 h2 = .486
F(2,44) = 1.334 p = .274 h2 = .060
Stride time (s)
0% 5% 30%
0.839 0.050 1.039 0.103 1.189 0.110
0.837 0.075 1.114 0.180 1.242 0.160
F(1,22) = 0.996 p = .330 h2 = .045
F(2,44) = 48.802 p = .001 h2 = .689
F(2,44) = 1.197 p = .312 h2 = .054
Lead swing (s)
0% 5% 30%
0.335 0.028 0.417 0.037 0.480 0.044
0.325 0.024 0.483 0.099 0.549 0.080
F(1,22) = 4.317 p = .050 h2 = .171
F(2,44) = 111.220 p = .001 h2 = .841
F(2,44) = 6.358 p = .004 h2 = .232
Trail swing (s)
0% 5% 30%
0.332 0.018 0.444 0.042 0.520 0.058
0.320 0.029 0.432 0.049 0.493 0.059
F(1,22) = 1.328 p = .262 h2 = .059
F(2,44) = 140.521 p = .001 h2 = .870
F(2,44) = 0.329 p = .721 h2 = .015
Total double support (s)
0% 5% 30%
0.173 0.023 0.180 0.038 0.191 0.038
0.192 0.030 0.198 0.050 0.200 0.048
F(1,22) = 1.283 p = .269 h2 = .055
F(2,44) = 1.510 p = .235 h2 = .064
F(2,44) = 0.271 p = .714 h2 = .012
None of the children failed more than once. Children demonstrated fairly consistent behaviour, using a fixed lead foot in 83% (DCD) and 84% (TD) of all cases (no differences between conditions), hence all trials were included in subsequent analysis. 3.1. Spatiotemporal variables of the crossing stride The obstacle had a significant effect on gait velocity and stride time in both groups (see Table 2 for means and statistics). Post hoc tests revealed a reduction in gait velocity and a lengthening of stride time with increasing obstacle height. The increase in stride time was the result of longer lead and trail swing times in the obstacle conditions. A significant group and interaction effect for lead swing time seemed to indicate larger values and a greater lengthening of swing duration in children with DCD, but the post hoc test failed to reach significance. Double support time did not
differ between groups and was unaffected by the obstacle. There were no differences between obstacle conditions for total stride length. Inspection of separate steps revealed that in both groups a level walking step was shorter than the lead step but longer than the trail step. The lead step was longer than the trail step during obstacle crossing irrespective of height. Finally, lead step width was greater in the 5% condition compared to both the 0% and the 30% condition (Table 3). No main effect of group or interaction effect was observed. 3.2. Approach and crossing parameters Approach and clearance distances did not differ between the obstacle conditions or groups (Table 3 and Fig. 2). Lead and trail clearance height increased as a function of obstacle height but there was no difference between groups. Analysis of the SD of toe-
Table 3 Means, standard deviations and statistical outcome of the repeated measures ANOVA for the approach and crossing parameters of the crossing stride. Condition
TD-children
Children with DCD
Group
Obstacle
Group Obstacle
Step width 1 (m)
0% 5% 30%
0.148 0.022 0.159 0.026 0.148 0.018
0.151 0.031 0.171 0.027 0.142 0.014
F(1,22) = 0.181 p = .657 h2 = .008
F(2,44) = 7.026 p = .002 h2 = .242
F(2,44) = 1.312 p = .279 h2 = .056
Step width 2 (m)
0% 5% 30%
0.151 0.019 0.159 0.020 0.152 0.023
0.155 0.023 0.160 0.026 0.168 0.026
F(1,22) = 3.006 p = .097 h2 = .120
F(2,44) = 2.169 p = .141 h2 = .090
F(2,44) = 0.353 p = .705 h2 = .016
Approach distance (m)
5% 30%
0.395 0.037 0.416 0.063
0.432 0.057 0.396 0.082
F(1,22) = 0.202 p = .658; h2 = .009
F(1,22) = 0.193 p = .665; h2 = .009
F(1,22) = 2.903 p = .102; h2 = .117
Clearance distance (m)
5% 30%
0.207 0.053 0.203 0.037
0.177 0.039 0.186 0.034
F(1,22) = 2.440 p = .129; h2 = .102
F(1,22) = 0.095 p = .381; h2 = .035
F(1,22) = 0.800 p = .381 h2 = .035
Lead clearance height (m)
0% 5% 30%
0.025 0.002 0.120 0.040 0.117 0.036
0.025 0.003 0.130 0.048 0.143 0.042
F(1,22) = 1.765 p = .198 h2 = .074
F(2,44) = 113.484 p = .001 h2 = .838
F(2,44) = 0.986 p = .381 h2 = .043
Trail clearance height trail (m)
0% 5% 30%
0.025 0.002 0.189 0.050 0.216 0.048
0.025 0.003 0.186 0.036 0.207 0.054
F(1,22) = 0.140 p = .712 h2 = .006
F(2,44) = 265.176 p < .001 h2 = .923
F(2,44) = 0.109 p = .897 h2 = .005
[(Fig._2)TD$IG]
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Fig. 2. Foot placement variability (standard deviation) and approach distance of the final three steps before the obstacle in the two obstacle conditions.
[(Fig._3)TD$IG]
Fig. 3. Maximal medio-lateral velocity of the COM (left panel) and medio-lateral range of motion of the COM (right panel) during the crossing stride.
obstacle distances revealed a significant effect of step number (F(2,44) = 74.532, p < .001, h2 = .772), indicating a gradual decrease of spatial variability during the approach. No differences between groups or interaction effects were found. 3.3. Centre of mass (Fig. 3) Maximal medio-lateral velocity of the COM was significantly greater in children with DCD (F(1,22) = 7.892, p = .010, h2 = .264) and increased as a function of obstacle height (F(2,44) = 4.813, p = .013, h2 = .180) in both groups. Additionally, higher obstacles led to greater medio-lateral ROM (F(2,44) = 417.455, p = .001, h2 = .454), but there was an interaction effect (F(2,44) = 3.638, p = .035, h2 = .148) such that the increase in medio-lateral ROM was larger in children with DCD. 4. Discussion The study set out to gain insight into the visuomotor and balance limitations during walking in children with DCD. This was achieved by comparing gait adaptations in children with DCD and typically developing children when crossing obstacles of different height. It was found that both groups approached the obstacle at equal speeds, which were slower than overground walking. Both groups crossed the obstacle using a similar technique, which involved lengthening the distance of the lead step and shortening the trail step. Consistent with a typical visual control strategy of the final steps before negotiating an obstacle, there was a similar approach distance and decrease in spatial variability of the final steps. Further support for
satisfacory visual guidance was evident in the finding of adequate scaling of lead and trail foot clearance. Still, despite there being a comparable obstacle negotiation strategy between the groups, differences were found in the timing of the crossing stride. There was an increase in the duration of lead swing as a function of obstacle height, which was more pronounced in children with DCD. In addition, this group demonstrated greater medio-lateral motion of the COM, indicating difficulty with the maintenance of dynamic balance. Collectively, these findings suggest that while children with DCD exhibit well-controlled gait adaptations during the approach and crossing, they experience stability problems with the increased balance demands. According to earlier research, inappropriate foot placement before the obstacle is the primary reason for failure in a crossing task [20]. Here, the decrease in foot placement variability exhibited by both groups of children as they approached the obstacle, in combination with a constant approach distance, reflects a typical visual guidance strategy aimed at achieving optimal foot positioning. Furthermore, the finding of equal clearance heights across conditions in both groups are consistent with appropriate scaling of limb elevation [19,25]. Together, the observed gait adaptations suggest satisfactory anticipatory control and adequate visual guidance of the locomotor pattern in both groups. It appears, then, that the real challenge in this obstacle crossing task was related to the control of balance. In both groups, crossing the obstruction resulted in longer swing times of the lead and trail limb and these extended phases of single support were accompanied with larger medio-lateral COM sway velocities. However, in children with DCD medio-lateral ROM of the COM when crossing the highest
F.J.A. Deconinck et al. / Gait & Posture 32 (2010) 327–331
obstacle was almost double that of walking overground and significantly larger than in TD-children. This large increase (up to 6 cm in the 30% condition) is a clear manifestation of a difficulty arresting the lateral sway momentum in challenging obstacle crossing conditions. Moreover, in previous gait studies of people with stroke or elderly with vestibular hypofunction, these COM motion parameters were found to be good discriminators between individuals with and without balance problems [7,8]. It is also interesting to note that (lead) swing times of the children with DCD tended to be longer than those of TD-children. From our analysis, it is not clear whether this is related to problems controlling the trajectory of the swinging limb or an outcome of balance deficits in the supporting leg. However, previous research of the gait pattern of children with DCD has shown increased shank motion variability occurred primarily during stance [15]. This suggests that walking and obstacle crossing in children with DCD are limited mainly by an underlying dynamic balance problem during single support. A number of limitations should be acknowledged when interpreting the results of this study including the relatively small sample size. While many of the children with DCD have visuomotor and balance problems, extrapolation of these findings should be done with care. Also, recordings of centre of pressure and data from more strides preceding and following the obstacle could provide a more comprehensive picture of gait adaptations. In conclusion, the spatiotemporal adjustments of typically developing children and those with DCD prior to and during crossing an obstacle did not differ, which suggests accurate visual control and planning in both groups. However, children with DCD did experience more difficulty with the increased balance constraints imposed when confronting an obstacle. Apparently, when moving through a cluttered environment, children with DCD have more problems with the control of dynamic balance than with the implementation of visually guided adaptations to the gait pattern. Acknowledgements This study was supported by a special research grant from Ghent University (BOF 01112902). Many thanks goes to all who have contributed to this study, especially the children and their parents. We also thank Emma Hodson-Tole and Simon Bennett for their useful comments on this manuscript. Conflicts of interest statement The authors hereby declare that, in writing this manuscript, there is no conflict of interest or any financial or personal relationship with other people or organisations that could have influenced the presented work inappropriately. References [1] American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 4th edition, Washington, DC: American Psychiatric Press; 1994.
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[2] Cairney J, Hay JA, Faught BE, Hawes R. Developmental coordination disorder and overweight and obesity in children aged 9–14 y. Int J Obesity 2005;29:369–72. [3] Wilson PH, McKenzie BE. Information processing deficits associated with developmental coordination disorder: a meta-analysis of research findings. J Child Psychol Psych 1998;39:829–40. [4] Wilmut K, Wann J. The use of predictive information is impaired in the actions of children and young adults with Developmental Coordination Disorder. Exp Brain Res 2008;191:403–18. [5] Chou LS, Kaufman KR, Brey RH, Draganich LF. Motion of whole body’s centre of mass when stepping over obstacles of different heights. Gait Posture 2001;13:17–26. [6] Patla AE, Prentice SD, Robinson C, Neufeld J. Visual control of locomotion strategies for changing direction and for going over obstacles. J Exp Psychol Human 1991;17:603–34. [7] Chou LS, Kaufman KR, Hahn ME, Brey RH. Medio-lateral motion of the center of mass during obstacle crossing distinguishes elderly individuals with imbalance. Gait Posture 2003;18:125–33. [8] Chou LS, Kaufman KR, Walker-Rabatin AE, Brey RH, Basford JR. Dynamic instability during obstacle crossing following traumatic brain injury. Gait Posture 2004;20:245–54. [9] Brown LA, Gage WH, Polych MA, Sleik RJ, Winder TR. Central set influences on gait—age-dependent effects of postural threat. Exp Brain Res 2002;145:286– 96. [10] Chen HC, Ashton-Miller JA, Alexander NB, Schultz AB. Stepping over obstacles—Gait patterns of healthy-young and old adults. J Gerontol 1991;46: M196–203. [11] Law LSH, Webb CY. Gait adaptation of children with cerebral palsy compared with control children when stepping over an obstacle. Dev Med Child Neurol 2005;47:321–8. [12] Rogers HL, Cromwell RL, Newton RA. Association of balance measures and perception of fall risk on gait speed: a multiple regression analysis. Exp Aging Res 2005;31(2):191–203. [13] Deconinck FJA, De Clercq D, Van Coster R, Oostra A, Dewitte G, Savelsbergh GJP, et al. Sensory contributions to balance in boys with developmental coordination disorder. Adapt Phys Act Q 2008;25:17–35. [14] Deconinck FJA, De Clercq D, Savelsbergh GJP, Van Coster R, Oostra A, Dewitte G, et al. Differences in gait between children with and without developmental coordination disorder. Motor Control 2006;10:125–42. [15] Rosengren KS, Deconinck FJA, DiBerardino LA, Polk JD, Spencer-Smith J, De Clercq D, et al. Differences in gait complexity and variability between children with and without Developmental Coordination Disorder. Gait Posture 2009;29:225–9. [16] Cherng RJ, Liang LY, Chen YJ, Chen JY. The effects of a motor and a cognitive concurrent task on walking in children with developmental coordination disorder. Gait Posture 2009;29:204–7. [17] Deconinck FJA, De Clercq D, Savelsbergh GJP, Van Coster R, Oostra A, Dewitte G, et al. Visual contribution to walking in children with Developmental Coordination Disorder. Child Care Health Dev 2006;32:711–22. [18] Sigmundsson H, Hansen PC, Talcott JB. Do ‘clumsy’ children have visual deficits? Behav Brain Res 2003;139:123–9. [19] Lee DN, Lishman JR, Thomson JA. Regulation of gait in long jumping. J Exp Psychol Human 1982;8:448–59. [20] Patla AE. Understanding the roles of vision in the control of human locomotion. Gait Posture 1997;5:54–69. [21] Patla AE, Greig M. Any way you look at it, successful obstacle negotiation needs visually guided on-line foot placement regulation during the approach phase. Neurosci Lett 2006;397:110–4. [22] Henderson SE, Sugden DA. Movement assessment battery for children: manual. London: Psychological Corporation; 1992. [23] Mickelborough J, van der Linden ML, Richards J, Ennos AR. Validity and reliability of a kinematic protocol for determining foot contact events. Gait Posture 2000;11:32–7. [24] Jensen RK. Body segment mass, radius and radius of gyration proportions of children. J Biomech 1986;19:359–68. [25] McFadyen BJ, Malouin F, Dumas F. Anticipatory locomotor control for obstacle avoidance in mid-childhood aged children. Gait Posture 2001;13:7–16.
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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Balance problems during obstacle crossing in children with Developmental Coordination Disorder F.J.A. Deconinck a,c,*, G.J.P. Savelsbergh a,b, D. De Clercq c, M. Lenoir c a
Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan University, UK Research Institute MOVE, VU University Amsterdam, The Netherlands c Department of Movement and Sports Sciences, Ghent University, Belgium b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 19 August 2009 Received in revised form 27 May 2010 Accepted 29 May 2010
The present study investigated the visuomotor and balance limitations during obstacle crossing in typically developing (TD) children and those with Developmental Coordination Disorder (DCD) (7–9 years old; N = 12 per group). Spatiotemporal gait parameters as well as range and velocity of the centre of mass (COM) were determined in three conditions: overground walking at a self-selected speed, crossing a low obstacle and crossing a high obstacle (5% or 30% of the leg length, respectively). Both groups walked more slowly during obstacle crossing than walking over level ground. In addition, both groups exhibited a significant decrease in the spatial variability of their foot placements as they approached the obstacle, which was then negotiated with a similar strategy. There were no differences in approach distance, length of lead and trail step, or lead and trail foot elevation. Compared to walking over level ground, obstacle crossing led to a longer swing phase of the lead and trail foot and increased maximal mediolateral COM velocity. In children with DCD, however, medio-lateral COM velocity was higher and accompanied by significantly greater medio-lateral COM amplitude. In conclusion, the results indicate that while TD-children and those with DCD exhibit satisfactory anticipatory control and adequate visual guidance, the latter group have a reduced ability to control the momentum of the COM when crossing obstacles that impose increased balance demands. Crown Copyright ß 2010 Published by Elsevier B.V. All rights reserved.
Keywords: Developmental Coordination Disorder (DCD) Gait Balance Anticipation Obstacle crossing Perceptuo-motor control
1. Introduction Children with Developmental Coordination Disorder (DCD) experience difficulties acquiring and performing motor skills, which then inhibits participation in physical activities and puts them at risk of long-term health and psycho-social problems [1,2]. DCD is not caused by a known neurological or physical pathology and has a prevalence rate of about 6% in 5–11-year-old children [1]. The clumsy motor behaviour associated with DCD is thought to originate from perceptual deficits [3] and problems involving feedback and/or feedforward control mechanisms [4]. However, it remains unclear if, and how, these deficits in motor control contribute to the completion of daily activities. In this study, we compare obstacle crossing behaviour in a group of children with DCD and a group of typically developing children. Obstacle crossing is examined because it demands precise postural and
* Corresponding author at: Institute for Biomedical Research into Human Movement and Health, Manchester Metropolitan University, John Dalton Building, Oxford Road, Manchester M1 5GD, United Kingdom. Tel.: +44 0161 247 5532; fax: +44 0161 247 6375. E-mail address: [email protected] (F.J.A. Deconinck).
balance control using perceptually driven anticipatory adjustments. (e.g. [5,6]). In this respect, a detailed examination of the gait pattern and the motion of the centre of mass during obstacle crossing can elucidate to what extent these perceptuo-motor systems limit ambulation in children with DCD. Research into obstacle crossing in the elderly or in individuals following traumatic brain injury highlights the particular role of balance control during this task. It has been shown that imbalance leads to an increase in amplitude and velocity of medio-lateral centre of mass (COM) motion and a suppression of gait adaptations that are inherent to obstacle crossing, but may render the body unstable (e.g. increased separation of COM, and centre of pressure, COP) [7,8]. In combination, excessive COM motion and failure to make the required gait adaptations could lead to an increased incidence of falling. To compensate, participants with low balance confidence exhibit a larger safety margin for foot clearance, wider base of support, slower velocity during the approach, and smaller step length [9–12]. Problems with postural control have been suggested to explain the a-typical gait pattern of children with DCD [13], which is characterised by shorter steps, greater trunk inclination, decreased ankle flexion and more variable thigh and shank movement than typically developing (TD) children [14,15]. Such behavioural adaptations when walking in children with DCD have been shown
0966-6362/$ – see front matter . Crown Copyright ß 2010 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2010.05.018
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328 Table 1 Information on the participants of both groups.
n Age Gender Length Body weight Physical activity MABC percentile
Children with DCD
Children without DCD
12 7.8 0.5 years 10 boys/2 girls 126.8 4.9 cm 25.6 4.4 kg 4.3 1.8 h/week 5.0 3.8
12 7.7 0.6 years 10 boys/2 girls 127.5 0.6 cm 25.6 3.4 kg 4.8 1.8 h/week 78.3 17.3
Note: MABC is Movement Assessment Battery for Children.
to demand a greater reliance on visual information [16,17]. However, given the reported visuomotor difficulties [3] and decreased visual sensitivity [18] in children with DCD, it is possible that the increased demand for precise visual information on distance and height of an obstacle [19–21] could limit the performance of a stable and adaptive gait. This may be manifested in poor anticipatory planning during the approach (with increased spatial variability and/or inappropriate foot positioning) and more unsuccessful crossings. In this way, children with DCD could be particularly vulnerable to the balance constraints imposed when confronting an obstacle, possibly leading to more cautious behaviour and excessive COM motion in medio-lateral direction during the crossing phase. In summary, the aim of this study was to examine visuomotor and balance limitations during obstacle crossing in typically developing (TD) children and those with Developmental Coordination Disorder (DCD). Given the documented difficulties with balance and visual perception, children with DCD were expected to demonstrate more signs of instability and less accurate foot positioning leading to more unsuccessful crossings. 2. Methods 2.1. Participants 12 children with DCD (age 7–9) and 12 TD-children participated in the study (see Table 1 for details). The children with DCD were free from co-morbid neurodevelopmental disorders as diagnosed by a neuro-paeditrician after a multidisciplinary assessment of their neurological health, motor skills, psychological behaviour and intellectual capacities. Their motor competence was tested with the Movement Assessment Battery for Children, which is a norm-referenced basic motor abilities assessment tool containing fine motor, ball handling, and balance tasks [22], and was indicated to be well below average (all children < 15th percentile, 7 children < 5th percentile). The TD-children with normal motor proficiency were matched on gender, age, body length, weight and nature and degree of physical activity. Details of the matching procedure are reported elsewhere [13]. The experimental protocol was in accordance with the guidelines of the Declaration of Helsinki and approved by the Ethical Committee of the Ghent University Hospital (ref.: 2002/041). 2.2. Materials and procedure Children were instructed to walk along a 9.6 m walkway, which was surrounded by eight ProReflex infrared cameras operating at a sampling frequency 240 Hz
[(Fig._1)TD$IG]
(Qualisys, Gothenburg, Sweden; Fig. 1). The experiment consisted of three walking conditions: (1) level walking without an obstacle (0%), (2) crossing a low obstacle of height equal to 5% of the leg length (3.5 cm on average), and (3) crossing a high obstacle of height equal to 30% of the leg length (16.6 cm). The obstacle was a rod, loosely attached to two stands at either side of the walkway. The obstacle was placed 4.5 m from the starting position throughout all trials. Reflective markers were attached bilaterally to 16 anatomical landmarks: nail of big toe, caput of the fifth metatarsal, lateral malleolus, lateral epicondyle (femur), anterior superior iliac spine, acromion, lateral epicondyle (humerus), and styloid process (ulna). Additional markers were attached to the process of C7 and L5. Prior to the experiment a demonstration of each walking condition was given. Children were then instructed to walk barefoot at a self-selected, comfortable, and steady pace towards a giant puzzle located at the end of the walkway (used as a diversionary task to motivate children). In the obstacle conditions, children were asked to step over the rod without hesitation and while continuing to walk in a straight line. No directions were given regarding which leg should act as the lead leg and hence clear the obstacle first. Each walking condition was practiced twice before data collection commenced in order to ensure that the child understood and was able to perform the task. Five trials were recorded in each of the three walking conditions, with level walking and obstacle crossing completed in separate blocks. The 10 trials involving obstacle crossing were received in random order. 2.3. Dependent variables and analysis For each of the 15 trials, foot contact (FC) and foot off (FO) were determined based upon validated algorithms described in [23]. The three-dimensional position data were then smoothed with a Butterworth low-pass filter (cut-off: 10 Hz). Subsequent analysis was focused on the crossing stride, which included movement from final FC before the obstacle to the next FC of the same foot. The crossing stride thus comprised lead and trail limb clearance. For each crossing stride we extracted stride velocity, stride time and stride length. In addition, duration, length and width of the lead and trail step, as well as total double support time, were considered. Finally, approach and clearance distance (i.e., horizontal distance between obstacle and ankle of trail and lead foot, respectively), and clearance height for both limbs (i.e., vertical distance between obstacle and toe) were calculated. In order to evaluate consistency of anticipatory adjustments during the approach, withinsubject inter-trial variability (SD) of the obstacle-toe distance for the final threefoot contacts (step 3, 2, and 1) was calculated over five trials. For level walking, measures were based on one stride (starting with foot contact of the right foot) per trial halfway the walkway. Maximal vertical toe height during swing was taken as an alternative to obstacle clearance height. A 15-segment model based on Jensen’s developmental regression equations for relative segment masses and centres [24] was used to calculate the position of the centre of mass (COM) Medio-lateral range of motion (ROM) and maximal velocity of the COM were calculated as measures of dynamic balance during the crossing stride. To examine the effect of obstacle height, spatiotemporal and COM variables were submitted to separate two-way repeated measures ANOVA; Obstacle height [0%, 5%, 30%] Group [DCD, TD]. The exception was foot placement variability and approach distance, which were submitted to separate three-way repeated measures ANOVA; Step [ 3, 2, 1] Obstacle height [0%, 5%, 30%] Group [DCD, TD]. Greenhouse–Geisser adjustments were applied in the event that the sphericity assumption was violated. Main and interaction effects were further examined with Tukey’s HSD post hoc tests, and alpha level was set at p < .05.
3. Results There was no difference in success rate between the groups (DCD: 93.3% or 112/120 trials; TD: 96.6% or 116/120 trials). In the event of an error, this was caused by trail foot contact with the obstacle and was due to impulsiveness rather than incompetence.
Fig. 1. Schematic illustration of the task with indication of dependent variables approach and clearance distance.
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Table 2 Means, standard deviations and statistical outcome of the repeated measures ANOVA for the spatiotemporal parameters of the crossing stride. Condition
TD-children
Children with DCD
Group
Obstacle
Group Obstacle
Stride velocity (m/s)
0% 5% 30%
1.317 0.125 1.094 0.108 0.937 .0179
1.292 0.954 0.990 0.159 0.889 0.132
F(1,22) = 1.838 p = .180 h2 = .080
F(2,44) = 55.022 p = .001 h2 = .714
F(2,44) = 1.523 p = .230 h2 = .068
Stride length (m)
0% 5% 30%
1.100 0.087 1.119 0.118 1.098 0.130
1.072 0.093 1.071 0.108 1.023 0.136
F(1,22) = 1.393 p = .251 h2 = .062
F(2,44) = 1.833 p = .173 h2 = .080
F(2,44) = 0.782 p = .464 h2 = .036
Lead step length (m)
0% 5% 30%
0.558 0.054 0.605 0.056 0.627 0.066
0.541 0.050 0.608 0.065 0.641 0.093
F(1,22) = 0.775 p = .389 h2 = .036
F(2,44) = 11.990 p = 0.001 h2 = .363
F(2,44) = 1.748 p = .187 h2 = .077
Trail step length (m)
0% 5% 30%
0.542 0.054 0.513 0.069 0.470 0.055
0.531 0.045 0.463 0.066 0.441 0.055
F(1,22) = 1.729 p = .203 h2 = .076
F(2,44) = 19.869 p = 0.001 h2 = .486
F(2,44) = 1.334 p = .274 h2 = .060
Stride time (s)
0% 5% 30%
0.839 0.050 1.039 0.103 1.189 0.110
0.837 0.075 1.114 0.180 1.242 0.160
F(1,22) = 0.996 p = .330 h2 = .045
F(2,44) = 48.802 p = .001 h2 = .689
F(2,44) = 1.197 p = .312 h2 = .054
Lead swing (s)
0% 5% 30%
0.335 0.028 0.417 0.037 0.480 0.044
0.325 0.024 0.483 0.099 0.549 0.080
F(1,22) = 4.317 p = .050 h2 = .171
F(2,44) = 111.220 p = .001 h2 = .841
F(2,44) = 6.358 p = .004 h2 = .232
Trail swing (s)
0% 5% 30%
0.332 0.018 0.444 0.042 0.520 0.058
0.320 0.029 0.432 0.049 0.493 0.059
F(1,22) = 1.328 p = .262 h2 = .059
F(2,44) = 140.521 p = .001 h2 = .870
F(2,44) = 0.329 p = .721 h2 = .015
Total double support (s)
0% 5% 30%
0.173 0.023 0.180 0.038 0.191 0.038
0.192 0.030 0.198 0.050 0.200 0.048
F(1,22) = 1.283 p = .269 h2 = .055
F(2,44) = 1.510 p = .235 h2 = .064
F(2,44) = 0.271 p = .714 h2 = .012
None of the children failed more than once. Children demonstrated fairly consistent behaviour, using a fixed lead foot in 83% (DCD) and 84% (TD) of all cases (no differences between conditions), hence all trials were included in subsequent analysis. 3.1. Spatiotemporal variables of the crossing stride The obstacle had a significant effect on gait velocity and stride time in both groups (see Table 2 for means and statistics). Post hoc tests revealed a reduction in gait velocity and a lengthening of stride time with increasing obstacle height. The increase in stride time was the result of longer lead and trail swing times in the obstacle conditions. A significant group and interaction effect for lead swing time seemed to indicate larger values and a greater lengthening of swing duration in children with DCD, but the post hoc test failed to reach significance. Double support time did not
differ between groups and was unaffected by the obstacle. There were no differences between obstacle conditions for total stride length. Inspection of separate steps revealed that in both groups a level walking step was shorter than the lead step but longer than the trail step. The lead step was longer than the trail step during obstacle crossing irrespective of height. Finally, lead step width was greater in the 5% condition compared to both the 0% and the 30% condition (Table 3). No main effect of group or interaction effect was observed. 3.2. Approach and crossing parameters Approach and clearance distances did not differ between the obstacle conditions or groups (Table 3 and Fig. 2). Lead and trail clearance height increased as a function of obstacle height but there was no difference between groups. Analysis of the SD of toe-
Table 3 Means, standard deviations and statistical outcome of the repeated measures ANOVA for the approach and crossing parameters of the crossing stride. Condition
TD-children
Children with DCD
Group
Obstacle
Group Obstacle
Step width 1 (m)
0% 5% 30%
0.148 0.022 0.159 0.026 0.148 0.018
0.151 0.031 0.171 0.027 0.142 0.014
F(1,22) = 0.181 p = .657 h2 = .008
F(2,44) = 7.026 p = .002 h2 = .242
F(2,44) = 1.312 p = .279 h2 = .056
Step width 2 (m)
0% 5% 30%
0.151 0.019 0.159 0.020 0.152 0.023
0.155 0.023 0.160 0.026 0.168 0.026
F(1,22) = 3.006 p = .097 h2 = .120
F(2,44) = 2.169 p = .141 h2 = .090
F(2,44) = 0.353 p = .705 h2 = .016
Approach distance (m)
5% 30%
0.395 0.037 0.416 0.063
0.432 0.057 0.396 0.082
F(1,22) = 0.202 p = .658; h2 = .009
F(1,22) = 0.193 p = .665; h2 = .009
F(1,22) = 2.903 p = .102; h2 = .117
Clearance distance (m)
5% 30%
0.207 0.053 0.203 0.037
0.177 0.039 0.186 0.034
F(1,22) = 2.440 p = .129; h2 = .102
F(1,22) = 0.095 p = .381; h2 = .035
F(1,22) = 0.800 p = .381 h2 = .035
Lead clearance height (m)
0% 5% 30%
0.025 0.002 0.120 0.040 0.117 0.036
0.025 0.003 0.130 0.048 0.143 0.042
F(1,22) = 1.765 p = .198 h2 = .074
F(2,44) = 113.484 p = .001 h2 = .838
F(2,44) = 0.986 p = .381 h2 = .043
Trail clearance height trail (m)
0% 5% 30%
0.025 0.002 0.189 0.050 0.216 0.048
0.025 0.003 0.186 0.036 0.207 0.054
F(1,22) = 0.140 p = .712 h2 = .006
F(2,44) = 265.176 p < .001 h2 = .923
F(2,44) = 0.109 p = .897 h2 = .005
[(Fig._2)TD$IG]
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Fig. 2. Foot placement variability (standard deviation) and approach distance of the final three steps before the obstacle in the two obstacle conditions.
[(Fig._3)TD$IG]
Fig. 3. Maximal medio-lateral velocity of the COM (left panel) and medio-lateral range of motion of the COM (right panel) during the crossing stride.
obstacle distances revealed a significant effect of step number (F(2,44) = 74.532, p < .001, h2 = .772), indicating a gradual decrease of spatial variability during the approach. No differences between groups or interaction effects were found. 3.3. Centre of mass (Fig. 3) Maximal medio-lateral velocity of the COM was significantly greater in children with DCD (F(1,22) = 7.892, p = .010, h2 = .264) and increased as a function of obstacle height (F(2,44) = 4.813, p = .013, h2 = .180) in both groups. Additionally, higher obstacles led to greater medio-lateral ROM (F(2,44) = 417.455, p = .001, h2 = .454), but there was an interaction effect (F(2,44) = 3.638, p = .035, h2 = .148) such that the increase in medio-lateral ROM was larger in children with DCD. 4. Discussion The study set out to gain insight into the visuomotor and balance limitations during walking in children with DCD. This was achieved by comparing gait adaptations in children with DCD and typically developing children when crossing obstacles of different height. It was found that both groups approached the obstacle at equal speeds, which were slower than overground walking. Both groups crossed the obstacle using a similar technique, which involved lengthening the distance of the lead step and shortening the trail step. Consistent with a typical visual control strategy of the final steps before negotiating an obstacle, there was a similar approach distance and decrease in spatial variability of the final steps. Further support for
satisfacory visual guidance was evident in the finding of adequate scaling of lead and trail foot clearance. Still, despite there being a comparable obstacle negotiation strategy between the groups, differences were found in the timing of the crossing stride. There was an increase in the duration of lead swing as a function of obstacle height, which was more pronounced in children with DCD. In addition, this group demonstrated greater medio-lateral motion of the COM, indicating difficulty with the maintenance of dynamic balance. Collectively, these findings suggest that while children with DCD exhibit well-controlled gait adaptations during the approach and crossing, they experience stability problems with the increased balance demands. According to earlier research, inappropriate foot placement before the obstacle is the primary reason for failure in a crossing task [20]. Here, the decrease in foot placement variability exhibited by both groups of children as they approached the obstacle, in combination with a constant approach distance, reflects a typical visual guidance strategy aimed at achieving optimal foot positioning. Furthermore, the finding of equal clearance heights across conditions in both groups are consistent with appropriate scaling of limb elevation [19,25]. Together, the observed gait adaptations suggest satisfactory anticipatory control and adequate visual guidance of the locomotor pattern in both groups. It appears, then, that the real challenge in this obstacle crossing task was related to the control of balance. In both groups, crossing the obstruction resulted in longer swing times of the lead and trail limb and these extended phases of single support were accompanied with larger medio-lateral COM sway velocities. However, in children with DCD medio-lateral ROM of the COM when crossing the highest
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obstacle was almost double that of walking overground and significantly larger than in TD-children. This large increase (up to 6 cm in the 30% condition) is a clear manifestation of a difficulty arresting the lateral sway momentum in challenging obstacle crossing conditions. Moreover, in previous gait studies of people with stroke or elderly with vestibular hypofunction, these COM motion parameters were found to be good discriminators between individuals with and without balance problems [7,8]. It is also interesting to note that (lead) swing times of the children with DCD tended to be longer than those of TD-children. From our analysis, it is not clear whether this is related to problems controlling the trajectory of the swinging limb or an outcome of balance deficits in the supporting leg. However, previous research of the gait pattern of children with DCD has shown increased shank motion variability occurred primarily during stance [15]. This suggests that walking and obstacle crossing in children with DCD are limited mainly by an underlying dynamic balance problem during single support. A number of limitations should be acknowledged when interpreting the results of this study including the relatively small sample size. While many of the children with DCD have visuomotor and balance problems, extrapolation of these findings should be done with care. Also, recordings of centre of pressure and data from more strides preceding and following the obstacle could provide a more comprehensive picture of gait adaptations. In conclusion, the spatiotemporal adjustments of typically developing children and those with DCD prior to and during crossing an obstacle did not differ, which suggests accurate visual control and planning in both groups. However, children with DCD did experience more difficulty with the increased balance constraints imposed when confronting an obstacle. Apparently, when moving through a cluttered environment, children with DCD have more problems with the control of dynamic balance than with the implementation of visually guided adaptations to the gait pattern. Acknowledgements This study was supported by a special research grant from Ghent University (BOF 01112902). Many thanks goes to all who have contributed to this study, especially the children and their parents. We also thank Emma Hodson-Tole and Simon Bennett for their useful comments on this manuscript. Conflicts of interest statement The authors hereby declare that, in writing this manuscript, there is no conflict of interest or any financial or personal relationship with other people or organisations that could have influenced the presented work inappropriately. References [1] American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 4th edition, Washington, DC: American Psychiatric Press; 1994.
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