Kyvelidou, Anastasia MS; Harbourne, Regina T. PT, PhD, PCS; Stergiou, Nicholas PhD
INTRODUCTION AND PURPOSE
During the development of sitting in early infancy, weight may shift within the base of support because of emerging motor control skills, active exploration of postural control strategies, or body, arm, and head movement used to respond to or explore the environment. The existing literature on infant sitting postural control includes kinematic and electromyographic analyses to describe sitting posture.1,2 Prior to independence in sitting, infants present high variation in the recruitment patterns of muscle activation. However, these variations decrease over time, enabling the selection of the most appropriate muscle synergy and the development of sitting.2 These synergies in infants developing typically (TD) while learning to sit can be viewed as a progression from an in-phase (moving in the same direction) to an out-of-phase (moving in an opposite direction) coordinative relationship between the thorax and the pelvis segments.1 Infant sitting postural adjustments have also been investigated during reaching,3 and it has been found that the development of postural changes during reaching while sitting presented a nonlinear and prolonged path.3 Recently, postural sway investigation has also been used to investigate sitting postural control.4,5 In one of those previous experiments,5 the infants sat on an inclined bicycle seat with a rigid back that restricts infant movement and masks the true nature of the infant sitting pattern. However, Harbourne and Stergiou4 investigated the development of sitting in infants who were healthy without restricting the postural behavior by exploring the variability present in center of pressure (COP) data, and they identified nonlinear behavioral characteristics.
Movement variability can be viewed and interpreted differently, depending on the theoretical perspective of motor control.6 Hierarchical theorists suggest that variability is an error in the control system that operates like a thermostat to keep the temperature at a preferred value. From this perspective, the goal of postural control in sitting would be to return to the optimal point of stability with slight variation around that point. In contrast, recently, theories such as dynamical systems and perception-action, and the hypothesis of an optimal state of variability6 propose that variability benefits the organism by facilitating the exploration of the environment. Thus, the goal of postural control in sitting would be to explore diverse movement solutions by swaying within the stability limits.6 Furthermore, recent literature from several disciplines, including brain function and disease dynamics, have shown that many biological phenomena are the result of nonlinear interactions and have deterministic origins.7 As such, behavior that was previously considered as an error, that is, slight variations in postural sway, may provide important information regarding the system that produced it. Such information can further our goal of improving intervention for children with posture and movement problems. For example, an infant with delayed sitting postural control may receive a different intervention depending on the theoretical perspective of the therapist regarding variability.8 A therapist who believes that variability of postural sway is an error in the system will then try to support the infant in biomechanical alignment (such as a supportive seat) and avoid variable sitting behavior. Conversely, a therapist who views postural variability as an inherent, healthy behavior will facilitate a more explorative type of treatment in which the infant experiences multiple postural strategies and is allowed to select sitting positions that may not be considered optimal by the therapist. However, to determine which approach better promotes the acquisition of functional sitting skill, there is a need for a quantitative and objective experimental paradigm that will test not only how much variability an infant exhibits but also the pattern or structure of the variable behavior.
In an attempt to uncover both properties of infant sitting posture, Harbourne and Stergiou4 investigated the development of sitting by using linear and nonlinear parameters derived from COP data based on the dynamical systems perspective. Linear methods include measures from traditional statistics, such as range and root mean square, and provide insight regarding the amount of variability present in a COP time series. Alternatively, nonlinear methods provide insight on the temporal organization or structure of the variability present in the data by examining the patterns and the order that exist in COP data.6 Nonlinear methods were found to be sensitive in detecting subtle changes occurring during the normal maturation process of infants during sitting.4 Since there is a method that can objectively quantify sitting posture in infants, the next logical step would be to investigate whether this experimental paradigm, proposed by Harbourne and Stergiou,4 can differentiate types of postural behavior in infants who are developing typically or who have different types of movement or postural disorders. Quantification of postural control can lead to improved intervention for children with posture and movement problems.
Currently, a child with developmental delay (DD) is identified by abnormal neurological signs along with high-risk factors occurring around birth, scores obtained on developmental screening tests, or visual analysis of their movement quality. However, currently available tests have several drawbacks. These tests vary in their specificity and sensitivity9 and are incomplete in predicting progress or developmental outcome for an individual child.10 They may be useful only at a specific age11 or may measure progress by assessing only large changes in motor skills, without being precise enough to provide information regarding rate of acquisition of skill on a short-term basis. It should be noted that although these tests have been presented to be reliable methods of describing development and detecting DD, they are still subjective tests. Moreover, a diagnosis of cerebral palsy (CP) for a child with DD is often delayed until the age of 2 years because many of the usual clinical signs may be transient.12,13 Therefore, postural control measurements may be useful in helping to differentiate the degree of severity (developmentally delayed, CP) of the disability in infants between the ages of 4 months and 2 years, such as in the sitting postural development paradigm proposed by Harbourne and Stergiou.4 This paradigm is useful because of the simplicity of the model as well as the analytical method proposed. The experimental design of this paradigm requires the infant to sit on a force plate, as if sitting on the floor, thus the risk is minimal for the infant and the collection of data is accomplished without difficulty. In addition, the mathematical analysis of the COP data investigates infant sitting postural development from 2 different perspectives, including amount and structure of variability, which provides a constellation of features inherent in each infant's sitting posture. As a result, the investigation of sitting postural control by using linear and nonlinear measures of the COP data promises to give insight into the individual differences that describe the severity of disability in an infant and that may make the infant distinct from others with a similar clinical presentation.
Therefore, the purpose of the present study was to identify measures of variability from sitting postural sway that are significantly different among infants with typical development, DD, and infants with CP. A secondary goal was to identify types of postural sitting behavior that will be of importance to physical therapists when designing intervention for infants with DD or with CP. We hypothesized that linear and nonlinear measures of sitting postural sway variability could differentiate between infants with dissimilar severity of disability as well as describing different types of postural behavior among these 3 groups of infants. Ultimately, these measures may be useful in the identification of infants who would benefit from different types of early intervention as well as in the evaluation of various therapeutic protocols.
Thirty-five infants developing typically (mean age, 152.4 ± 8.9 days or 5.1 ± 0.3 months; gender, 18 boys and 17 girls), 11 infants with DD (mean age, 360.3 ± 74.8 days or 12 ± 2.5 months), and 19 infants with DD or hypotonia who later on had a diagnosis of spastic or athetoid CP (mean age, 486.8 ± 175.1 days or 16.2 ± 5.8 months) participated in this study (Table 1). Infants were recruited from employee announcements at the campus of the University of Nebraska at Omaha and at the Munroe-Meyer Institute of the University of Nebraska Medical Center, as well as from early intervention programs and therapists from the University of Nebraska Medical Center and the surrounding area. Before data collection commenced, the parents of the infants provided informed consent that was approved by the university human research ethics committee.
The inclusion criteria for entry into the study for the infants developing typically were as follows: (a) a score on the Peabody Developmental Motor Scale-2, Gross Motor Quotient within 0.5 SD of the mean; (b) age between 5 and 7 months; and (c) sitting independently with or without the use of hands. The exclusion criteria for the infants developing typically were as follows: (a) a score on the Peabody Developmental Motor Scale-2, Gross Motor Quotient of greater than 0.5 SD below the mean; (b) diagnosed visual deficits; or (c) diagnosed musculoskeletal problems. Inclusion criteria for the infants with either CP or DD were as follows: (a) age from 7 months to 2 years; (b) score less than 1.5 SD below the mean for their corrected age on the Peabody Developmental Motor Scale-2, Gross Motor Quotient; and (c) sitting independently even with the use of hands. Exclusion criteria for infants with DD were as follows: (a) age 2 years or older; (b) a score greater than 1.5 SD below the mean for their corrected age on the Peabody Developmental Motor Scale-2, Gross Motor Quotient; or (c) a diagnosed visual impairment, or a diagnosed hip dislocation or subluxation of greater than 50%.
Experimental Design and Protocol
Each infant participated in 2 sessions. The first session lasted for 45 minutes and was used to perform the Peabody Developmental Motor Scale-2. This standardized test is norm- and criterion-referenced and examines gross motor function in children from birth to 83 months. The second session, an experimental session, took place within a week of the first session.
For the experimental session, the infants were allowed time to get used to the laboratory setting and were at their parent's side or on the parent's lap for preparation and data collection. A standard set of infant toys was used for distraction and comfort. All attempts were made to maintain a calm, alert state by allowing the infant to eat if hungry, be held by a parent for comforting, or have the temperature of the room adapted to the infant's comfort level. After the child was undressed by the mother (only diapers on), 2 sets of triangles with 1 reflective marker in each corner were glued with a double-face tape in 2 locations (Figure 1a). However, the marker data were not analyzed for this study.
The infants were then placed by their parent on the top of a force plate that was covered with a special pad for warmth, which was securely adhered with tape on the force plate. The infant was held in the sitting position in the middle of the plate when calm and happy (Figure 1b). The investigator and the parent remained at 1 side and in front of the infant, respectively, during all data collection to ensure that the infant did not fall or become insecure. The child was held at the thorax for support, and gradually the infant was guided into a prop sitting position while being distracted by toys presented by the parent or the examiner. Once the examiner could completely let go of the infant, data were collected continuously while the child attempted to maintain postural control (Figure 1b). Trials were performed until 3 trials were obtained that were acceptable for our criteria (see later) or until the infants were indicating that they were done. At any time the child became irritated, the data collection was halted for comforting by the parent, or a chance for feeding, and then resumed only when the child was again in a calm state.
For data acquisition, infants sat on an AMTI force plate (Watertown, Massachusetts), interfaced to a computer system running Vicon data acquisition software (Lake Forest, California). The COP data from both the anterior-posterior (AP) and the medial-lateral (ML) directions were acquired through the Vicon software at 240 Hz to be above a factor of 10 higher than the highest frequency contained in the signal. No filtering was performed on the data because such a procedure can affect the nonlinear results.14 Video of each trial was collected using 2 Panasonic recorders (model 5100 HS) interfaced with a Panasonic Digital AV Mixer (model WJ-MX30). The cameras were positioned to record a sagittal and a frontal view of the subject (Figures 1a and 1b). See the online video, available at http://links.lww.com/PPT/A14 for a demonstration of 2 trials for an infant with CP.
Three acceptable trials (8.3 seconds) were selected from the videotape recording, using the following criteria: (a) infant did not move the arms (not reaching, holding an object, or flapping his or her arms), (b) infant did not vocalize or cry, (c) infant was not in the process of falling, (d) trunk was not inclined more than 45° to either side, (e) not being touched, and (f) the arm position (propping or not propping) of the infant was noted during the entire trial and only trials in which the infant used a consistent base of support were used.
Linear measures of the variability present in postural sway were calculated from the selected trials, using customized MatLab software (Mathworks, Natick, Massachusetts) from the COP time series, based on the methodology of Prieto et al.15 The linear measures calculated were the root mean square and the maximum minus minimum (range) for the AP and the ML directions, as well as the length of the path traced by the COP (sway path). These parameters were selected according to Chiari et al,16 and they are all independent of the effect of biomechanical factors, such as weight, that changes dramatically during development. These linear measures characterized the amount of variability present in the COP data.6
In addition, 3 nonlinear measures of variability were calculated from the selected trials: the approximate entropy, the largest Lyapunov exponent (LyE), and the correlation dimension for both the AP and the ML directions. Rather than quantifying the magnitude of variability as linear measures do, nonlinear measures are sensitive to temporal ordering in the data. Nonlinear measures of the variability present in postural sway were calculated from the COP time series as described by Harbourne and Stergiou,4 and the methodology of these calculations have been published previously.17,18
All results from the individual trials and experimental sessions were averaged for each infant and for all linear and nonlinear parameters. A 1-way analysis of variance with a test for linear trend was performed for comparisons among groups. A Tukey multiple comparison post hoc analysis was used to identify the location of the significant differences for all tests resulting in a significant F ratio. The α level for significance was set at .05.
Range in the ML direction (F2,62 = 3.276, P = .044) and sway path (F2,62 = 7.620, P = .001) presented significant differences among groups of infants. No significant differences were found for range in the AP direction and root mean square in the AP and ML directions. Post hoc analysis revealed that range in the ML direction was significantly different between infants developing typically and those with CP (Figure 2), with CP infants presenting smaller values than those with TD. For sway path, the post hoc analysis revealed significant differences between the group of infants developing typically and of the group of infants with CP, as well as between the group of infants with DD and the group with CP. No differences were found between the group of infants developing typically and the group with DD. Infants with CP had lower sway path values than infants developing typically or those with DD (Figure 3). Finally, no statistically significant trend was found in any of the linear parameters examined.
The LyE for the AP (F2,62 = 4.912, P = .01) and the ML (F2,62 = 3.618, P = .033) directions presented significant differences among groups of infants. No significant differences were found for the approximate entropy and the correlation dimension in the AP and ML directions. Post hoc analysis revealed that the LyE for the AP direction was significantly different between infants developing typically and those with CP (Figure 4). Infants with CP presented smaller LyE values than those developing typically. The post hoc analysis of the LyE for the ML direction revealed significant differences between infants developing typically and those with CP (Figure 5). Again, infants with CP presented smaller LyE values than those developing typically. No differences were found between the group of infants developing typically and that of infants with DD, nor were differences found between the group of infants with DD and that of infants with CP. Finally, there was a statistically significant linear trend for LyE in both the AP (F2,62 = 8.742, P = .004) and the ML (F2,62 = 7.009, P = .01) directions.
For all linear and nonlinear variables that presented statistically significant differences, more than 60% of the children followed the group findings.
The purpose of the present study was to identify measures of variability in sitting postural sway that are significantly different among infants developing typically, those with DD or hypotonia, and those with spastic or athetoid CP. We hypothesized that linear and nonlinear measures of sitting postural sway variability differentiate infants with varying degrees of disability as well as describe different types of postural behavior among these 3 groups of infants, and this hypothesis was supported. Two linear (range in the ML direction and sway path) and 2 nonlinear (LyE in the AP and ML directions) parameters presented significant differences between infants developing typically and infants with CP, whereas these same variables did not show a significant difference between infants developing typically and infants with DD.
A secondary goal was to identify types of postural sitting behavior that are of importance to physical therapists when treating infants with DD or with CP. Infants developing typically and those with DD present similar amounts of variability as described by the range variable, whereas infants with CP have a reduced amount of range. Our analysis indicated that range, specifically in the ML direction, was decreased in infants with CP. These results suggest that infants with CP, who acquire the sitting skill, present a rather stiff posture, especially in the ML direction, indicating a particular lack of variability for movement within the frontal plane. Another linear variable, sway path, indicated decreased amount and velocity of movement adjustments of the COP in infants with CP as compared with the infants developing typically or who demonstrate DD. Thus, both range in the ML direction and velocity of changes in the path of the COP could be the focus of intervention in infants with CP who are learning to sit.
In addition, the temporal organization of postural sitting behavior declined with increasing severity of the motor disorder from those developing typically to those with DD to the infants with CP. Infants developing typically had more divergence in the postural sway trajectories (higher LyE values), which indicates greater adaptability and flexibility to achieve the sitting skill by choosing from a wealth of postural solutions. In contrast, infants with DD were less flexible than infants developing typically (smaller LyE values; Figures 4 and 5), whereas infants with CP were the least flexible. Infants with CP seem to lock into a very limited repertoire of postural solutions, which makes it difficult to adapt to changing environmental conditions and to sit independently. If we consider that infants developing typically are behaving in a more optimal state of variability, then the severity of the condition pushes the system further away from this behavior and this optimal state.8 Interventions could target a transition toward this optimal state by incorporating environmental challenges and enhancing postural solutions. This may then enhance adaptability and flexibility.8
By characterizing the temporal organization of the variability present in the COP patterns (ie, nonlinear analysis) or, in other words, how the movement evolves over time, we were able to show how the postural sway of infants with DD is different from infants developing typically and those with CP. The significant linear trend of LyE in both the AP and ML directions suggests that infants developing typically are able to maintain their sitting posture successfully when internal perturbations affect the dynamics of the system. Decreasing values of LyE across groups of DD suggests decreased dynamic control and ability to explore the environment in contrast with infants with no delay who show optimal dynamic control. Therefore, in terms of early intervention approaches, therapists should be enhancing exploration of multiple postural behaviors to make the behavior of both infants with DD and infants with CP more diverse and thus adaptable to different conditions.
There are a few limitations that need to be acknowledged. First, because we enrolled infants just as they were able to sit upright, the groups of infants with DD and with CP were older than the infants developing typically. The difference in age may contribute to differences in postural strategies. However, our assessments of motor skills ensured a similar entry point in the research study. Another limitation was that we did not include infants who had mild delays (between 0.5 and 1.5 SD from the mean in the Peabody Development Scale-2, Gross Motor Quotient) and inclusion of these infants may alter the findings. We plan to explore such infants in future studies. We realize that these are the very children who are a dilemma for the health care professionals and those working in early assessment clinics. Furthermore, because nonlinear measurement tools require the use of mathematical equations and software to evaluate time-series data, nonlinear analysis is primarily performed in research settings. This makes the translation of the concepts to the clinic more difficult. However, we anticipate that in the future, improvements in and the decreasing cost of technology will allow such devices to become more prevalent and that clinical decision making will incorporate technical advances, such as nonlinear measures of time-series data, to determine optimal intervention and the success of these interventions. It is possible that these procedures will be used with a portable force platform to improve assessment within the home and outside of the clinic. The cost of such equipment will likely be offset by the benefits of improvements in the prognosis and intervention approaches.
This research determined that linear and nonlinear analyses of COP time series during sitting in infants developing typically, with DD, or with CP could be a useful, objective, and quantitative method of distinguishing between different degrees of DD and types of postural behaviors. Therefore, the evaluation of sitting postural control by using linear and nonlinear tools to analyze COP time series appears to be a viable method for the early quantification of postural control. This method can be used to document incremental changes in sitting postural control that may result from interventions for infants with motor deficiencies. In addition, our findings have additional clinical implications, supporting the notion that therapists should encourage variability and multiple postural strategies during intervention designed to address goals related to sitting independence.
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activities of daily living/sitting; biomechanics; cerebral palsy/diagnosis; cerebral palsy/physiopathology; developmental disabilities/diagnosis; developmental disabilities/physiopathology; human movement system; infant; nonlinear dynamics; physical therapy/methods; postural balance/physiology; posture/physiology
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