Abstract
Background Postural instability is a classical characteristic of cerebral palsy (CP), but it has not been examined during functional play activity. Recent work has demonstrated that when motor tasks are made functionally more relevant, performance improves, even in children with movement pathology. It is possible that in a disease state, the underlying control mechanisms that are associated with healthy physiology must be elicited.
Objective The study objective was to explore the utility of the functional play task methodology as a more rich and interpretable approach to the quantification of postural instability in children with CP.
Design Postural stability measures obtained from a cross-sectional cohort of children with CP (n=30) were compared with stability measures taken from children with typical development (n=30) during a single measurement period.
Methods Postural stability data were obtained with a portable force platform system. Postural sway was quantified during a precision manual functional play task. A baseline condition (no task) also was included. Postural sway variability and postural sway regularity were analyzed with analyses of variance.
Results There was an apparent difference in postural control (greater irregularity, greater sway variability) during quiet stance between children with CP and peers with typical development; this difference was mitigated during the performance of the precision functional play task.
Limitations A small and nonprobability sample of convenience may limit the findings of this study.
Conclusions The findings illustrate flexibility and adaptability in the postural control system despite the pathological features associated with CP.
Cerebral palsy (CP) has been found to be associated with disruptions in postural control and subsequent postural instability. Postural control during quiet (ie, unperturbed) stance in CP has also been studied. During quiet stance, children with CP typically exhibit a larger amount of postural sway (eg, greater sway area and path length) than children with typical development (TD), and their postural sway typically is more variable.1–5 Additionally, children with CP have been described as exhibiting temporal patterns of postural sway distinct from those of children with typical development, reflecting a decrease in the postural sway irregularity that is believed to be an indicator of less effective physiological control.6
An inherent assumption underlying the large body of work on postural stability in CP is that during quiet stance, the priority is to reduce postural sway variability to the greatest extent possible. However, stance is not achieved and maintained solely for its own sake but rather is achieved and maintained to facilitate goal-directed tasks that are superordinate to (above and beyond) the control of posture (functional play or suprapostural tasks).7 Examples of functional play (suprapostural) tasks include everyday activities such as standing while holding a lunch tray, writing on a chalkboard, or swinging a baseball bat. Coordination of postural control with a functional play task may require the modulation of postural sway to avoid interfering with and, in some cases, to directly facilitate functional play activity. In the context of functional play activity, the postural control system must coordinate the physical demands of posture with the functional requirements of the task.8 The success of postural control, therefore, can be defined in terms of its impact on the achievement of functional play goals.9 As such, no singular description of postural control can be used to characterize a “healthy” system or a system that is not healthy.
Because functional play tasks are everyday activities, studying postural activity during functional play task performance may be a way to achieve the functional context necessary to develop a more applicable and valid understanding of postural control.7 This consideration is especially critical in studies of the movement behavior of children with impairments given that differences between children who are healthy (controls) and children with neurological impairments could indicate, in part, a change in postural control strategies10,11 or constraints,8 rather than simply a decline in the function of the postural control system. Although the pattern of movement used to successfully complete a task may be atypical in populations with established motor deficiencies, it may not be ineffective.12,13
Recent work by Volman et al14 illustrated the influence of functional context on motor behavior in CP. Children with CP reached to press a light switch to turn on a light (functional task context), reached to press the light switch without turning on the light (semifunctional task context), or reached to a marker (nonfunctional task context). Reaching kinematics were improved in the functional task context, indicating that when a task is functionally more relevant, motor performance will be more precise and less variable, even in children with movement pathology. These findings are buttressed by those of other clinical studies in which task context was manipulated by varying object availability and object affordances. For example, after a cerebrovascular accident, people produced smoother, faster, and more forceful movements when reaching for their favorite food or for an active telephone instead of a spatial location or a stick.15 Additionally, mimicking of a task (pretending to eat food in a saucer with a spoon) resulted in motor performance that was less efficient and kinematically different than actual task performance (eating applesauce in a saucer with a spoon) in patients with multiple sclerosis.16
Comprehensively, these studies illustrated that different motor behaviors can emerge in task-relevant conditions. The purpose of this study was to investigate postural stability in children with CP during the performance of a functional play task that engendered a more functional context for balance control than quiet stance. Specifically, we evaluated postural control during a functional play task that required precise control of manual activity in a cohort of children with CP and peers who were matched for age and exhibited TD. We hypothesized that if the functional play task context used in this study promoted dynamic functioning of the postural control system, the postural sway irregularity associated with CP6 and other differences in postural behavior between children with CP and children with TD would be attenuated during the performance of a functional play task. Modulating control strategies in response to suprapostural task constraints could reflect a system with adaptability—a response to the constraints imposed by functional play tasks,8 despite a pathological state.17 Such a response reveals aspects of motor control that might remain intact in children with CP.
Method
Design and Participants
Cross-sectional measures of postural stability during functional play task performance were obtained from a cohort of 60 children (30 children with CP [mean age=8.30 years, SD=2.26]; 30 children with TD [mean age=9.20 years, SD=1.98]). Children with CP were referred for participation in this study from a large, nonprofit academic pediatric medical center in the Midwest. Children with TD were invited to participate through convenience sampling methods.
To be included in this study, all children were required to be between 5 and 12 years of age and to able to stand independently for 1 minute. None of the study participants had additional medical comorbidities known to affect postural stability. To minimize the musculoskeletal effects of interventions on stability measures, children with CP qualified for participation in this study only if they had not undergone surgical intervention 12 months before the test date or Botox (onabotulinumtoxinA, Allergan Inc, Parsippany, New Jersey) injections within 3 months of the test date. All children with CP were characterized by spasticity. Sample descriptors are summarized in the Table.
Characteristics of the Samplea
Procedure
All participants began this study by completing six 20-second quiet-stance trials. In these trials, no functional play task was performed. These trials were conducted to identify any baseline postural control differences between children with TD and children with CP.
To facilitate the engagement of children participating in this study, animal puppets were mounted to a steadiness tester. Their mouths surrounded 5 circular copper tubes of different sizes, each one 1.25 cm smaller than the previous one (smallest diameter=3.75 cm). Participants were informed that the animals on the device did not feel well and that, as the doctor in this study, they could help to determine whether a specified animal was sick by checking its temperature. This task was accomplished by asking the children to position a wooden thermometer (12.7 cm long, 2.5 cm wide, and 1.9 cm deep) with a 5-cm metal tip (stylus length) in the animal's mouth and to maintain the thermometer's position in the center of the mouth for the duration of the trial. If the stylus inadvertently came in contact with the perimeter of the copper tube, a low-voltage circuit was completed and a feedback light in the center of the tester was illuminated; the device functions like the children's game Operation (Hasbro, Pawtucket, Rhode Island) but uses a light in lieu of a buzzer. The device was vertically oriented on a height-adjustable table so that each participant performed the task while standing with 90 degrees of shoulder flexion, full elbow extension, and neutral forearm/wrist alignment. So that postural control could be examined during functional activity, the functional play task was performed while the children were standing on a force platform (Fig. 1).
Study procedure. Study participants completed a functional play aiming task while postural sway data were collected from a force platform.
A within-subject manipulation of functional play task difficulty (easy versus hard) was included to vary the demands placed on postural control by the functional play task. Before data collection, participants were asked to position the stylus of the thermometer in a tube on the steadiness tester without touching the perimeter for 10 seconds. The smallest “animal mouth” for which each child was able to successfully perform the task was used in hard task conditions. An animal mouth 2 sizes larger was used in easy task conditions. This procedure established relative task difficulty for each child participating in the study. All children were minimally able to complete the task in the 5-cm tube for 10 seconds without error.
Easy and hard functional play task conditions were repeated 3 times, yielding a total of 6 randomly ordered 20-second trials for each participant (in addition to the quiet-stance trials). All children demonstrated task awareness, followed instructions, and were able to complete all trials of the precision task within a 10-minute period.
Outcome Measures
Postural data were obtained with an AMTI AccuSway PLUS portable force platform system (Advanced Mechanical Technology Inc, Watertown, Massachusetts). The accuracy and reliability of ground reaction force data collected by static posturography in children with CP have been well documented.18 Data were sampled at 100 Hz in 20-second trials to ensure that each time series was represented by an adequate number of points for the proposed analyses.19 Balance Clinic software (Advanced Mechanical Technology Inc) was used to acquire force and moment data sampled by the force platform and to calculate the center of pressure (COP), the point location of the resultant ground reaction forces acting at the feet, in both the anteroposterior (AP) and the mediolateral (ML) axes of motion. Standard assessments of postural stability included measurement of the within-trial standard deviation of the AP and ML COP. Higher values for COP variability are widely assumed to reflect reduced postural stability. Sample entropy (SampEn)19 was used to provide measures of order and regularity in the COP data. SampEn is the negative natural logarithm of an estimate of the conditional probability that a subseries that repeats itself for m points also will match at the next point (m+1). Accordingly, lower SampEn values reflect self-similarity or regularity in the time series—an indication that the data did not arise from a random process. SampEn has been used to quantify tolerance in COP time series and has been proven to be a useful tool for studying the dynamics of postural stability.20 Balance Clinic and customized MATLAB (The MathWorks Inc, Natick, Massachusetts) routines were used to compute COP metrics from the recorded COP time series. All static posturography trials were conducted in barefoot conditions, without the aid of ankle-foot orthoses.
Data Analysis
Preliminary exploration of the data with a Levene test21 indicated that samples of children with CP and children with TD did not reflect an equality of variance. Subsequently, data in this study were subjected to a monotonic, variance-stabilizing square root transformation.
Postural sway measures collected during static trials and functional play task trials were averaged over repeated trials of the same experimental condition for each participant to yield one average value for each dependent measure in each experimental condition. These values were submitted to repeated-measures analyses of variance for each dependent variable (sway variability and SampEn in both the AP and the ML planes) to examine the fundamental impact of the functional play task. The effects of quiet stance (group), task performance (group, task/no task performance), and the task modifier of difficulty (group, easy task/difficult task performance) were analyzed separately. For all analyses, an alpha level of .05 was used to establish statistical significance.
Results
Quiet-Stance Trials
Baseline postural variability and regularity analyses from the quiet-stance trials indicated significant group differences, both in the standard deviation of the COP and in SampEn in all planes tested. In the AP plane, the standard deviation of the COP was significantly higher for children with CP than for children with TD (F1,29=58.53, P<.05). The ML plane COP standard deviation also was significantly higher for children with CP than for children with TD (F1,28=85.75, P<.05). In quiet stance, children with CP demonstrated greater irregularity in the AP plane than children with TD (F1,28=28.04, P<.05). This group difference also was observed in the ML plane (F1,28=44.77, P<.05).
Functional Play Task Trials
Standard deviation of the COP.
Two-way mixed-factor analyses of variance revealed main effects of group (F1,28=53.11, P<.05) and task (F1,28=40.73, P<.05) and a group × task interaction for the standard deviation of the COP (F1,28=31.02, P<.05) in the ML plane. Similar main effects of group (F1,28=78.91, P<.05) and task (F1,28=6.57, P<.05) were found in the AP plane, but the interaction was not significant in this plane (P>.05). Simple effects analysis of the interaction in the ML plane revealed a functional play task effect (less sway during task performance than in the no-task condition) that was significant for children with CP (P<.05) but not for peers with TD (P>.05). Moreover, a group difference in the standard deviation of the COP existed in the no-task condition—the standard deviation was higher for children with CP than for children with TD (P<.05)—but the difference was attenuated during the precision-task condition (P>.05) (Fig. 2).
Standard deviation (SD) and 95% confidence interval for the center of pressure (COP) in the functional play task analysis. Significant main effects of task and group in the mediolateral (ML) plane (top) and anteroposterior (AP) plane (bottom) and a significant group × task interaction in the ML plane (top) were observed. During precision-task performance, sway variability decreased in children with cerebral palsy (CP) but not in peers with typical development (TD). Significant group differences that existed during no-task conditions were mitigated during precision-task performance.
The analysis of task difficulty (easy versus hard) revealed main effects of group (F1,28=3.65, P<.05) and task difficulty (F1,28=12.49, P<.05) and a group × task difficulty interaction for the standard deviation of the COP (F1,28=9.49, P<.05) in the ML plane. Only a main effect of group was found in the AP plane (F1,28=43.41, P<.05). Simple effects analysis of the interaction in the ML plane indicated that children with TD altered their sway variability as a function of task difficulty (P<.05); there was less sway variability in hard conditions than in easy conditions. This trend was not observed in children with CP, who demonstrated relatively stable sway variability across conditions (P>.05). A difference between children with CP and peers with TD (higher standard deviation for children with CP) was detected only in hard conditions (P<.05) (Fig. 3).
Standard deviation (SD) and 95% confidence interval for the center of pressure (COP) in the difficulty analysis. Significant group effects in the mediolateral (ML) plane (top) and anteroposterior (AP) plane (bottom), a significant difficulty effect in the ML plane (top), and a significant group × difficulty interaction in the ML plane (top) were observed. Children with typical development (TD) demonstrated less sway variability during hard conditions. Sway variability for children with cerebral palsy (CP) was not altered as a function of task difficulty. Significant TD and CP group differences were detected only during hard conditions.
SampEn of the COP.
Two-way mixed-factor analyses of variance also revealed main effects of group (ML: F1,28=33.19, P<.05; AP: F1,28=17.97, P<.05) and task (ML: F1,28=75.97, P<.05; AP: F1,28=41.78, P<.05) and group × task interactions (ML: F1,28=24.07, P<.05; AP: F1,28=13.56, P<.05) for the SampEn of the COP in both planes. Simple effects analysis indicated that participants in both groups had a spatiotemporal profile with lower SampEn values (greater regularity) during functional play task performance than in the absence of that activity. The groups remained statistically different in either functional play task condition (children with CP exhibited greater irregularity), although during the functional play task, differences between the groups were reduced (mean differences in the ML plane were 0.09 bit for no task and 0.02 bit for task [P>.05]; mean differences in the AP plane were 0.13 bit for no task and 0.01 bit for task [P>.05]) (Fig. 4).
Sample entropy (SampEn) and 95% confidence interval for the center of pressure (COP) in the functional play task analysis. Significant main effects of task and group in the mediolateral (ML) plane (top) and anteroposterior (AP) plane (bottom) and significant group × task interactions in the ML plane (top) and the AP plane (bottom) were seen. Relative to those in no-task conditions, SampEn values decreased (became more regular) during performance of the precision task in both children with cerebral palsy (CP) and peers with typical development (TD). Group differences in no-task conditions remained significant but were mitigated during precision-task performance.
The analysis of task difficulty (easy versus hard) revealed a main effect of group only; children with CP exhibited higher SampEn values (more irregular COP patterns) in both the ML plane (F1,28=3.65, P<.05) and the AP plane (F1,28=19.86, P<.05) (Fig. 5).
Sample entropy (SampEn) and 95% confidence interval for the center of pressure (COP) in the difficulty analysis. Significant group × task interactions in the mediolateral (ML) plane (top) and anteroposterior (AP) plane (bottom) were observed. SampEn values were higher (more irregular) in children with cerebral palsy (CP) than in peers with typical development (TD) regardless of precision-task difficulty.
Discussion
We proposed that functional play task performance would create a functional context for postural control and a subsequent postural sway profile that would differ markedly from measures of quiet-stance postural control in children with CP. The hypothesis that differences between children with TD and children with CP would be attenuated during the functional play task was supported. Group × task interactions demonstrated differences in sway variability (CP > TD) and regularity (TD > CP) between groups in the no-task condition, but these differences were attenuated when participants performed the functional play task. Functional play task performance was accompanied by an increase in the regularity (CP and TD) of postural sway in both the AP and the ML planes and a decrease in the variability (CP) of postural sway in the ML plane. Like the findings of Riley et al,22 differential axis effects may be explained by the task specificity of the postural control system; in the present study, successful aiming performance was achieved through optimization of stability in the ML axis. Manipulation of task difficulty magnified the differences in variability between the 2 groups (the TD group demonstrated less sway variability in difficult conditions) but did not change the overall pattern of results.
The results of the present study, in part, were consistent with those of previous studies of postural control and functional play tasks. They validated the findings of greater sway variability in children with CP during quiet-stance trials1–5 and flexibility of postural control during functional play task performance.7,8,22,23 The SampEn findings in the present study were unanticipated. Cerebral palsy was expected to be associated with greater regularity of the COP profile, in alignment with the well-documented theory that disease is accompanied by predictably stereotypical physiological signals.6,24 The hypothesis was also in alignment with work by Donker et al,6 who reported that the COP profile of 5- to 11-year-old children with hemiparetic CP was associated with low SampEn values. In the present study, children with CP instead demonstrated higher SampEn values (greater irregularity) during quiet-stance trials. Moreover, the functional play task condition, which was expected to elicit a more typical physiological COP profile (greater irregularity), resulted in a COP profile of greater regularity in both children with CP and peers with TD. Vaillancourt and Newell25 argued, however, that depending on the interaction between task constraints and the constraints intrinsic to a given individual, disease-related changes in physiological and behavioral dynamics can occur in either direction—regularity can increase in some cases but decrease in others. They thus advocated for a “change in regularity” approach over a “loss of irregularity” approach.
The present study provides a compelling base of evidence to support the dynamic nature of the postural control system in children with a diagnosis widely associated with poor motor adaptability. However, it is not without limitations. The sample of children with CP in the present study was characterized by a heterogeneity of presentation (ie, gross motor function, development) and was not strategically chosen to ensure a correlation with population characteristics. The present study also was inadequately powered for a priori subgroup analyses (ie, by Gross Motor Function Classification System). We hypothesized that wide variability within the CP group would mask unique findings associated with different levels of disease severity or clinical presentation.
Despite unexpected baseline SampEn findings, the present study clearly demonstrated greater similarity between children with CP and peers with TD during the performance of a functional play task. The demonstration of flexibility in the postural performance of children with CP in the present study challenges the notion that people have a fixed, singular postural control system that either works well or does not. Instead, the findings support the theoretical position that control systems are assembled and disassembled to match current circumstances and constraints.8
The finding that children with CP in our sample demonstrated a functional play task effect is of great clinical significance, to the extent that levels of functioning during task performance were nearly equivalent in the 2 groups.26 Accordingly, the assertion that poor postural control in CP is the catalyst for later motor deficiencies is challenged by the results of the present study, which instead suggest that dynamic aspects of the postural control system and relationships with other sensorimotor behaviors are preserved in CP, allowing children with CP to function in ways that do not differ significantly from those of children with TD in some situations. In populations with established motor deficiencies, although the pattern of movement used to successfully complete a task may be atypical, it may not be ineffective.12,13,17 The modulation of postural control to facilitate the performance of a functional play task illuminates aspects of pathological motor control that were previously misunderstood.
Findings indicating that concurrent functional play tasks result in the modulation of postural control in some children with mild hemiparetic CP have significant implications for future research. A related, additional implication of the findings of the present study is that quiet stance may not be an appropriate task protocol for comparing participant groups with clinical conditions and TD. Postural control and functional play tasks are tightly intertwined. Studies with quiet stance might not accurately describe the pragmatic characteristics of postural control, and greater attention to the influence of the experimental method would be paramount in studies linking deficient postural control with subsequent disruptions in motor development in CP. Examining postural control in the context of functional play tasks should provide a clearer understanding of existing postural deficiencies associated with CP. More importantly, it also might expose aspects of motor control that remain intact in children with CP.
Footnotes
All authors provided concept/idea/research design. Dr J.M. Schmit, Dr Riley, and Dr Shockley provided writing and data analysis. Dr J.M. Schmit provided data collection. Dr J.M. Schmit and Dr Riley provided project management. Dr Riley provided facilities/equipment. Dr Riley, Dr Cummins-Sebree, Dr L. Schmitt, and Dr Shockley provided consultation (including review of manuscript before submission).
This study was approved by both academic and hospital institutional review boards.
- Received September 29, 2014.
- Accepted June 8, 2015.
- © 2016 American Physical Therapy Association
References
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