Abstract
Background Balance problems are common in children who have cerebral palsy (CP) but are active and ambulant. Control of the whole-body center of mass is critical in maintaining dynamic stability during challenging mobility tasks, such as clearing an obstacle while walking.
Objective The objective of this study was to compare trunk and lower limb kinematics and center-of-mass control in children with CP and those in children with typical development during obstacle crossing.
Design This was a cross-sectional study. Thirty-four children who were 5 to 17 years of age (17 with CP and 17 with typical development) and matched in age and height completed 2 gait trials involving crossing a 10-cm obstacle.
Methods Three-dimensional kinematic and kinetic data were captured with a general-purpose 3-dimensional motion tracking system and forceplates. Trunk data were captured with a validated model.
Results All children cleared the obstacle with similar hip and knee kinematics, step length, and single-support duration. In children with CP, step width was increased by 4.81 cm, and center-of-mass velocity was significantly slower at lead limb toe-off (0.31 m/s) and during lead limb clearance (0.2 m/s). Children with CP showed altered trunk and pelvis movement, characterized by significantly greater pelvic obliquity, pelvic tilt, and trunk rotation throughout the task, increased lateral trunk lean during lead limb crossing (3.7°), and greater sagittal trunk movement as the trail limb crossed (5.1°).
Limitations The study was not powered to analyze differences between children with diplegia and those with hemiplegia.
Conclusions Children with CP required greater adjustments at the trunk and pelvis to achieve successful obstacle crossing. The increase in trunk movement could have been compensatory for reduced stability distally or for a primary problem reflecting poor proximal control. The findings suggest that rehabilitation should focus on both proximal trunk control and distal stability to improve balance.
Successful community ambulation depends on the ability to adapt gait to the demands of the environment and diverse behavioral goals. The maintenance of dynamic stability of the moving body is inherent in this process.1,2 Balance impairment is a common complaint in children with cerebral palsy (CP), with underlying stability problems resulting from poor posture, delayed motor responses, inappropriate muscle sequencing, and increased coactivation of agonists and antagonists.3 Children who have CP but are active and ambulant ultimately aim to function as well as possible alongside their peers in their everyday environment. Gait in children with CP is commonly assessed over level ground in a spacious setting without distraction or physical obstruction; however, this approach does not evaluate their ability to adjust kinematics and the alignment and velocity of the center of mass (CoM) in anticipation of or in response to balance challenges, such as unexpected perturbations or obstructions. Analysis of gait in more challenging tasks is indicated to gain further insight into dynamic balance.
Obstacle crossing during gait is useful for evaluating dynamic balance because it demands precise postural and balance control through perceptually driven anticipatory adjustments.4 A comprehensive literature search revealed that obstacle crossing was studied previously in developmental coordination disorder,5 stroke,6,7 adults who were healthy,4 people who were elderly,8 Parkinson disease,9 and traumatic brain injury10; the aim in those studies was to explore dynamic balance strategies in these groups and, in some cases, to distinguish people at risk of falls.8 Obstacle crossing over a variety of heights—0%, 10%, and 20% of leg length—was evaluated in a group of 12 children with CP and 12 children with typical development (TD).11 Unsteadiness in children with CP was evident by changes in temporal-spatial parameters, including significant reductions in approach speed and crossing speed, and increased step width to broaden the base of support. The higher the obstacle, the more conservative the strategy.11 The kinematic adaptations that contributed to changes in temporal-spatial parameters, particularly the movement and control of the CoM, were not evaluated. This additional detail is of interest for understanding the underlying deficits so that in clinical practice, strategies to address rehabilitation goals for dynamic balance can be developed with a stronger scientific, evidence-based rationale.
Compensatory movement of the trunk is a common feature in people with impaired balance. In the absence of an effective ankle strategy to fine-tune alignment of the base of support, relatively large movements of the trunk are required to stabilize the CoM over the supporting foot. Children with CP show altered movement of the trunk that is not just compensatory for lower limb deficits but also a primary impairment in itself.12 Its importance may be greater in challenging tasks such as obstacle clearance. For example, there was no difference in rates of success in clearing obstacles of various heights in children with developmental coordination disorder and children with TD, and their temporal-spatial parameters were not significantly different.5 However, an analysis of the CoM revealed greater medial-lateral velocity and range of movement in developmental coordination disorder, indicating a lack of precision in control of the CoM and providing an assessment of the extent of the dynamic balance deficit.5 If the authors had not evaluated control of the CoM, then the results might have been insensitive to the balance problem.5 Similarly, Chou et al10 noted an increase in the range of movement and the medial-lateral velocity of CoM motion in adults with traumatic brain injury during obstacle crossing. In CP, segmental trunk control was found to explain 40% of the variation in the Gross Motor Function Measure, indicating a strong association between segmental trunk postural control and mobility.13 These data support the importance of incorporating trunk and CoM assessments in studies of dynamic balance (such as the present study), with the ultimate aim of informing treatment strategies related to community ambulation.
The objective of this study was to evaluate trunk and lower limb kinematic strategies and control of the CoM during obstacle crossing while walking in children who had CP but were active and independently mobile and in children who had TD and were matched for age, with the broader goal of understanding the factors contributing to dynamic balance impairment in children with CP.
Method
Study Design
This was a cross-sectional study comparing performance on a task—namely, obstacle crossing during gait—at a single point in time in children with CP and children with TD. Recruitment and data collection took place between June 2013 and March 2014.
Participants
Children who had CP and were 5 to 18 years of age were recruited from a large cohort attending outpatient rehabilitation services at the Central Remedial Clinic, Dublin, Ireland. Inclusion criteria were as follows: diagnosis of diplegia or hemiplegia; ambulant without the use of aids, including when crossing a 10-cm-high obstacle; and Gross Motor Function Classification System (GMFCS) level I or II. Potential participants were identified by their treating physical therapist between June 2013 and January 2014 and invited to participate. Children were excluded if they had undergone surgery within the year, had received botulinum toxin (onabotulinumtoxinA [Botox]; Allergan Inc, Irvine, California) within 3 months before the assessment, or had coexisting neurological or orthopedic conditions (other than CP) that might affect their gait. Children with TD volunteered to participate after a general email invitation to staff and colleagues at the clinic. A participant information leaflet was provided to parents and guardians of all children, and written informed consent was obtained. Children with TD were matched in age and height to children with CP.
Protocol
Three-dimensional kinematic and kinetic data were captured in a movement laboratory by use of a 14-m-long walkway, a Codamotion cx1 system (Charnwood Dynamics Ltd, Leicestershire, United Kingdom) with 4 Coda monitors and a sampling rate of 200 Hz, and 2 Kistler forceplates (600 × 400 mm; Kistler Instrument Corp, Amherst, New York) with a sampling rate of 400 Hz and aligned in series along the line of progression in the center of the walkway. Infrared light-emitting diodes were placed on each participant's lower limbs in accordance with the modified Helen Hayes model for gait kinematics14 and a previously described protocol15 as follows: anterior and posterior aspects of the pelvic frame aligned with anterior-superior and posterior-superior iliac spines, the lateral aspect of the knee flexion/extension axis, anteroinferior to the tip of the lateral malleolus, the head of the fifth metatarsal, and the lateral aspect of the calcaneus. Thigh and shank wands, with markers at anterior and posterior aspects, were fastened with self-adhesive straps at the femur and the tibia perpendicular to the femoral axis and to the transmalleolar axis, respectively.
Trunk data were captured with the Central Remedial Clinic trunk model, a single-cluster model shown to be valid and comparable to other models for measuring trunk kinematics.16 Figure 1 shows the full marker set. The lead author (A.M.) performed all aspects of marker placement, data capture, and subsequent processing.
Still images of a participant crossing the obstacle, set up as a hurdle between 2 cones, with the kinematic marker set and trunk cluster attached: (A) sagittal view, (B) coronal view.
A standard instruction was given to the children to walk at their usual (self-selected) pace from the start to the end of the walkway, crossing the obstacle in the center as they proceeded. The exact wording was modified depending on the age of the child. Each child completed 2 trials that involved crossing a 10-cm hurdle (fixed at this height for all participants) in stride. The first trial was used for analysis; the second trial was captured for backup in case of problems with light-emitting diode visibility or force capture. The obstacle was placed between the 2 consecutive forceplates to allow for the capture of lead and trail limb forces. The reliability of this protocol was described previously.17
Data Reduction
Three-dimensional gait analysis generates many possible variables for statistical analysis. Hypothesis testing of such a wide range of variables risks a type I statistical error. To avoid this problem, we reduced data to key points by examining features pertinent to obstacle crossing. Temporal-spatial analysis focused on speed, step length, single-support time, and step width. Lower limb kinematic analysis addressed the sagittal-plane requirements for safe obstacle clearance (hip flexion, knee flexion, and ankle dorsiflexion during swing) and the compensatory movement of hip abduction. Data for control of the trunk and pelvis indicated total movement in each plane. We conducted statistical analysis of trunk movement with respect to the pelvis, rather than with respect to the global coordinate system (the laboratory), to allow evaluation of the independent contributions of the pelvis and the trunk. Both sets of trunk kinematics were reported graphically.
Control of the CoM was described at 5 key points during the obstacle crossing in accordance with previous work.7 The relationship between the CoM and the supporting foot was evaluated by measuring the peak angle between the CoM and the center of pressure under the forceplate in the sagittal and coronal planes, as described by Feng et al18 and as shown in the eFigure.
Data Analysis
A sample size calculation was based on differences in gait speed between children with CP and children with TD from a large database of over 3,000 children at the clinic where the study took place. Gait speed over an obstacle was estimated to be 20% slower than gait speed over level ground, and we expected a difference of 0.2 m/s between children with TD and children with CP (exceeding the minimal clinically important difference of 0.13 m/s).19 Using the approach of Pocock,20 with a standard deviation of 0.2 m/s, a significance of .05, and a power of .8, we calculated a sample size of 34, with 17 children in each group.
Data were checked for normal distribution, graphically with box-and-whisker plots and quantitatively with tests of skewness and kurtosis and the Shapiro-Wilk test. Once normal distribution was verified, variables were compared between groups by use of the independent 2-tailed t test with 95% confidence intervals. Significance was set at a P value of .05. We did not perform a Bonferroni correction because of the known limitations of this approach.21 Analysis was performed with Stata 13 (StataCorp LP, College Station, Texas).
Role of the Funding Source
This project was funded, in part, by the Royal College of Surgeons in Ireland Research Summer School 2013.
Results
Thirty-four children were recruited: 17 with CP (10 with hemiplegia and 7 with diplegia) and 17 with TD. Of the 17 children with CP, 10 were boys and 7 were girls; of the 17 children with TD, 8 were boys and 9 were girls. The mean age of the children with CP was 10 years (SD=2 years 4 months), and that of the children with TD was 10 years 1 month (SD=3 years 8 months). There were no significant differences in age (P=.956), height (CP group=1.37 m [SD=0.14], TD group=1.4 m [SD=0.22], P=.623), or weight (CP group=32.8 kg [SD=11.6], TD group=37 kg [SD=16.8], P=.394) between the groups. The GMFCS levels were I for 14 children with CP and II for the remaining 3 children. All children were independently mobile without aids and could clear a 10-cm obstacle without assistance.
Clearance over the obstacle by the lead and trail limbs is shown in Table 1. All children cleared the obstacle successfully. There were no problems with light-emitting diode visibility, so the first trial was used for analysis in all cases. Children with hemiplegia (n=10) consistently led with their less affected limb. Children with CP showed higher toe clearance (11.1 cm) over the obstacle with the lead limb than children with TD, for whom the clearance was 8.58 cm (P=.02). Clearance over the obstacle was achieved with similar lead limb hip flexion and knee flexion, although trail limb hip flexion was 11 degrees higher in children with CP (P<.01). Compared with children with TD, children with CP lacked ankle dorsiflexion during swing for both lead limb (mean difference=2.8°; P=.05) and trail limb (mean difference=5.5°; P=.01). An increase in hip abduction during swing was found for both lead limb (4.2°; P=.01) and trail limb (4.9°; P<.01) in children with CP.
Characteristics of Clearancea
Table 2 shows the temporal-spatial parameters for the lead and trail limbs. Gait speed was lower in children with CP (0.78 m/s) than in children with TD (0.99 m/s) (P=.03). Step length and single-support duration were not different between the groups. Children with CP showed a significantly wider base of support, with a step width of 18.6 cm; the step width in children with TD was 13.8 cm (P=.03). Trail limb step length was shorter in children with CP, indicating that the trail limb came closer to the obstacle before crossing. Single-support durations were similar in both groups, as were lead limb step lengths.
Temporal-Spatial Characteristicsa
The kinematics of the trunk and pelvis are shown in Figure 2. Movements of the trunk and pelvis in the coronal and transverse planes were significantly different in children with CP; they were characterized by increased total excursion of pelvic obliquity, pelvic tilt, and trunk rotation of both lead and trail limbs, with increased lateral trunk lean during lead limb crossing and greater sagittal-plane trunk movement as the trail limb crossed (Tab. 3).
Kinematic graphs, normalized as a percentage of gait cycle time (x-axis), for trunk and pelvis movement of lead and trail limbs during obstacle crossing. Trunk data are shown with respect to (wrt) the pelvis and with respect to the laboratory (Lab) (indicating the net orientation of the trunk). Data for children with cerebral palsy are shown as dashed lines; the black dashed line denotes the mean, and 1 standard deviation is denoted by the gray dashed lines. Data for children with typical development are shown as a solid gray line to denote the mean and a gray band to denote the standard deviation. The y-axis measurements are in degrees.
Trunk and Pelvis Movementa
Parameters describing control of the CoM during obstacle crossing are shown in Table 4. Instantaneous CoM velocity was slower in children with CP for 4 of the 5 key points in time during this task. The largest difference occurred at lead limb toe-off, indicating that the children with CP were significantly slower at this point. Sagittal and mediolateral inclination angles, denoting the orientation of the CoM with respect to the center of pressure, were not different between the groups.
Control of CoMa
Discussion
Children with CP successfully cleared a 10-cm obstacle in stride during walking at their self-selected speed; however, their strategy for achieving clearance differed from that of children with TD. The differences between the groups reflected the challenges faced by children with CP in devising an efficient motor strategy to clear the obstacle. They were capable of achieving peak hip and knee flexion similar to that of their peers with TD, but their strategy was compromised by the addition of cross-planar compensatory movements at the trunk, pelvis, and hip and excessively high foot clearance of the lead limb. The findings indicated both an impairment of trunk and pelvic control during the challenging single-limb support phase and a lack of selectivity and efficiency of movement of the swinging limb itself. The swinging limb was forced to use a movement amplitude larger than that used in normal gait to avoid hitting the obstacle; this larger amplitude imposed additional stability challenges on the stance limb.
Children with CP showed an inefficient lead limb strategy, characterized by significantly higher foot clearance over the obstacle. This excessive height might have resulted from a lack of selectivity that prevented children with CP from fine-tuning the most efficient multijoint pattern to ensure clearance. Difficulties with visual perception might also have contributed to this feature. A recent systematic review found a 40% to 50% prevalence of visual-perceptual impairment in children with CP across all GMFCS levels.22 Visual-perceptual ability might influence motor planning around activities of daily living in people with CP,23 and obstacle crossing could be impeded in the presence of a significant deficit. None of the children in our cohort had undergone tests of visual-perceptual function, so we cannot confirm this association; however, this topic is important for future research because it might have been a significant contributor to the deficits that we found.
Step length and single-support duration for both lead and trail limbs did not differ between the groups, unlike previous reports for these variables over level ground,24 but this finding was not surprising. It suggested that the obstacle task forced minimum step length and single-support duration in order to clear the obstacle successfully and avoid falling. It has been noted that for adults with CP, the primary concern in obstacle clearance is safety; in contrast, unobstructed walking, which is associated with a lower risk of falls, is influenced more by minimizing energy cost.25 Therefore, high clearance was prioritized over speed and efficiency.
These movement patterns reflected impaired control of the trunk in the unstable position of single-limb support while the contralateral limb cleared the obstacle. The coupling of movement between the pelvis and the trunk is an important part of the motor strategy for obstacle clearance. Children with CP often show a proximal-to-distal activation strategy, and their ankle muscles—critical for fine-tuning balance responses—are slower to activate than those of children with TD.3 This strategy has a significant impact on the trunk, yet deficits in trunk control are often underestimated. Recent research has shown that segmental trunk control has a strong association with gross motor function and mobility, with up to 40% of the variation in Gross Motor Function Measure scores being predicted by the results of a test of trunk control on linear regression.13 Furthermore, children with CP show excessive trunk movement during normal gait without an additional balance challenge.26 These features present a dual source of difficulty for children with CP when dealing with dynamically challenging tasks, such as obstacle crossing: they not only lack responsiveness and control distally at the contact point with the foot but also show impaired proximal control of the trunk, which is forced to compensate further to maintain a stable CoM.
Our results support the consideration that the rehabilitation of dynamic balance in children with CP should focus on both distal and proximal control and stability. Exercises that could be considered include those targeting control by the hip and ankle during single-limb support and those focusing on the deep abdominal muscles through active alignment and trunk control in various postures, such as standing, 4-point kneeling, and stability ball sitting.
The results of the present study showed that children who have CP and GMFCS level I or II and are independently mobile can change their kinematics when crossing an obstacle to avoid a fall but that doing so challenges their trunk control and stability. This task may be a more sensitive indicator of dynamic balance; therefore, incorporating it into a gait analysis protocol for children who have CP but are active and ambulant may be of value. Three-dimensional measurement of the kinematics and control of the CoM during obstacle crossing also may be useful as an outcome measure for evaluating changes in dynamic balance and postural stability in such children.
In measuring the effectiveness of rehabilitation, detecting changes in gait kinematics through an analysis of level-ground walking can be difficult, as found by Taylor et al in a well-designed and adequately powered randomized controlled trial of progressive resistance exercise27; however, in that case, the intervention was not specifically designed to target gait itself.28 A study of adults who had a stroke showed improvements in some aspects of obstacle crossing after 1 month of rehabilitation.6 The responsiveness to change of this task has not been assessed in people with CP, but our results suggest that this task shows promise in this regard, particularly if the rehabilitation intervention specifically targets dynamic trunk and postural control.
The methodological requirements of the present study imposed some limitations on its design and interpretation. The 10-cm fixed height of the obstacle required greater adaptations for clearance by children of shorter stature. To counteract this possible confounding variable, we matched the groups in age and height to ensure that there were no differences; any effect of height would have been evenly spread across the 2 groups. The 10-cm obstacle was an average of 7.3% of the participants' average height, with a standard deviation of 0.9% and an absolute range of ±1.8%. We considered such a low percentage variation unlikely to cause significant kinematic deviations. Furthermore, obstacles in the everyday environment are of a fixed size, so our approach provided a more realistic scenario than scaling the obstacle to individual participant height. With regard to anthropometrics, the nonsignificant, 4.2-kg mean difference in weight between the groups was unlikely to be important clinically because we did not report segmental kinetic data. Mean body mass indexes were similar between the groups (16.9 kg/m2 for children with CP and 17.7 kg/m2 for children with TD).
Both hemiplegia and diplegia were included in the present study because we considered it to be important to include all children who had spastic CP but were active and ambulant, regardless of motor type. Obstacle crossing is a task that requires whole-body coordination, and previous studies did not distinguish between hemiplegia and diplegia in the interpretation of trunk control because deficits in trunk control are common to both conditions13; however, it is true that children with diplegia generally exhibit a greater range of trunk movement during walking.26 The relatively equal distributions of diplegia and hemiplegia would have had a balancing effect. Furthermore, the present study was not powered at the outset to determine differences between the 2 motor types.
The inclusion of 3 children with GMFCS level II merits further discussion. When we set the objective of the present study a priori, our goal was to capture the most complete cohort of children who had CP but were active and independently ambulant in the community and likely to be participating in activities with their peers with TD in the everyday environment. All children who were recruited met this broad description, and all were able to cross a 10-cm obstacle unassisted during gait. Because this level of ability crosses into the milder presentations of GMFCS level II, we did not want to exclude children with GMFCS level II because the results also would have applied to them and they also were representative of the population in question. Therefore, we consider that our cohort of participants reflected a spectrum of ability related to community ambulation rather than a categorical distinction between GMFCS levels. This notion is reflected in the normal statistical distribution of the data.
The age range of the participants in the present study was large—5 to 18 years, with a mean of 10 years. We acknowledge that this range increased variability in the data; however, we included a large age range because we aimed to capture a cohort of children representative of those who are independently ambulant and active alongside their peers in the community but who experience balance difficulties. Had we excluded a range of ages to reduce variability, the results then could not be generalized to the excluded age groups, thereby affecting the relevance of the findings to the wider population of interest. The lower limit of 5 years was pragmatically based on the age at which children could adhere to the laboratory protocol. We acknowledge that balance would have been better developed in the older participants; however, the effect would have been minimized by the inclusion of a cohort of children who had TD and were carefully age matched for comparison.
In conclusion, children with CP required greater adjustments at the trunk and pelvis to achieve successful obstacle crossing. This finding reflected both impaired trunk control as a primary problem and compensatory strategies for reduced stability distally, particularly because obstacle crossing enforces longer single-support duration. Visual-perceptual difficulties and lack of selective motor control might have contributed to the differences in strategy.
The results of the present study provide a baseline for planning rehabilitation strategies to target deficits in dynamic balance during walking. Analysis of obstacle crossing might be more sensitive to changes in postural control than level-ground walking, which does not challenge stability as effectively. It could be used as a test in parallel with other clinical measures of balance to plan interventions and assess changes, particularly in trunk and CoM control.
Footnotes
Dr Malone provided concept/idea/research design, project management, and participants. Dr Malone and Ms Saunders provided writing. Dr Malone, Mr Kiernan, and Ms Saunders provided data collection and data analysis. Dr Malone and Dr French provided fund procurement and institutional liaisons. Dr Malone and Professor O'Brien provided facilities/equipment. Mr Kiernan and Professor O'Brien provided consultation (including review of manuscript before submission).
Ethics approval was granted by the Research Ethics Committee of the Central Remedial Clinic, Dublin, Ireland.
This project was funded, in part, by the Royal College of Surgeons in Ireland Research Summer School 2013.
- Received June 30, 2015.
- Accepted February 4, 2016.
- © 2016 American Physical Therapy Association