Continuous inter-limb coordination deficits in children with unilateral spastic cerebral palsy
Introduction
Continuous inter-limb coordination is the movement relationship between body limb segments (e.g., arm and leg)(Magill & Anderson, 2014) and is organized within the framework of environmental conditions, task demands, and limb dynamics.(Holt et al., 2000) With the exception of walking, performance of tasks following mutual direction of the limbs is more stable, and therefore preferred, to opposite limb movements in able-bodied persons.(Baldissera et al., 1982; Magill & Anderson, 2014) Additionally, moving homologous limbs (e.g., both arms or both legs simultaneously) is associated with greater intrinsic coordinative ability compared to non-homologous limbs (e.g., one arm and one leg).(Serrien & Swinnen, 1998)
Stability, the system’s ability to offset an internal or external perturbation(Li et al., 2005), is optimized during well-coordinated movements.(Meyns et al., 2013) Following an unexpected or self-triggered internal perturbation (i.e., walk to run transition), a healthy neuromuscular system quickly returns to a stable pattern. However, an unstable system, such as the impaired neuromuscular system associated with unilateral spastic cerebral palsy (USCP), may experience difficulty returning to a stable pattern post-perturbation. USCP is characterized by impaired movement coordination and muscle tone regulation, which affects motor function on one side of the body greater than the other.(Bax et al., 2005) Children with USCP experience deficits in bimanual coordination due to motor control abnormalities.(Uvebrant, 1988) The inability to effectively coordinate their limbs impacts functional independence and quality of life.(Gordon & Steenbergen, 2008) Although inter-limb coordination has been studied during discrete tasks,(Hung et al., 2004; Hung et al., 2011; Steenbergen et al., 2000; Sugden & Utley, 1995) only one study has investigated continuous, inter-limb coordination in children with USCP.(Meyns et al., 2012) It was reported that this population demonstrates poor inter-limb coordination compared to typically developing children (TDC) during walking(Meyns et al., 2012) and decreased stability originated from the more-affected arm, agreeing with findings from adult stroke studies.(Debaere et al., 2001; Garry et al., 2005) It is not known whether movement coordination and stability would be more impaired than TDC during a novel task, or whether it is amenable to treatment.
Two approaches to upper extremity treatments using motor learning concepts for children with USCP have shown strong efficacy, Constraint Induced Movement Therapy (CIMT)(Charles et al., 2001; Charles & Gordon, 2006; Gordon et al., 2005) and Bimanual Training (e.g., Hand Arm Bimanual Intensive Therapy (HABIT)).(Novak et al., 2020) Both CIMT and HABIT improve upper extremity function; however, HABIT demonstrates greater benefits to improving bimanual spatiotemporal coordination during a discrete task.(Hung et al., 2011) Coordination between the arms and legs may also improve after upper extremity intervention, as changes in lower extremity gait patterns have been reported in children with USCP when arm swing is manipulated (e.g., one or both arms restrained to trunk).(Delabastita et al., 2016) If upper extremity biomechanics change post-intervention, lower extremity biomechanics, and the upper-lower extremity interaction may consequently change to adjust to the new internal constraints. This is further supported by reports of gait pattern improvements after CIMT in this population (Coker et al., 2010; Zipp & Winning, 2012) and upper extremity movements driving appropriately coordinated, reciprocal movement of the lower extremity with spinal central pattern generators.(Ferris et al., 2006)
We previously evaluated gait inter-limb coordination with spatiotemporal measurements in children with USCP after either CIMT or HABIT.(Sidiropoulos et al., 2019) Although arm swing to stride ratio improved in both groups, there were no changes in lower extremity spatiotemporal patterns post-intervention. Limitations included the use of a well-practiced task (i.e., walking) and the fact that spatiotemporal analysis offers a “snapshot” of the gait cycle and vital information was most likely missed. Like most previous literature, our study primarily focused on discrete coordination by measuring peak movement at a given time. Continuous measures of relative phase analysis can overcome the shortfalls of spatiotemporal analysis because they quantify the phase relationship across movement cycles. (Hamill et al., 1999; Kelso, 1995) Relative phase analysis measures the interaction (i.e., phasing relationships) of two segments throughout a movement(Diedrich & Warren Jr, 1995; Scholz & Kelso, 1989; Winstein & Garfinkel, 1989) by merging displacement and velocity data to quantify coordination and stability.(Kurz and Stergiou, 2004)
The first aim of this study was to determine whether differences in continuous coordination and stability between children with USCP and TDC exist. We hypothesized that children with USCP would demonstrate a lower level of coordination and stability than TDC due to their neurologic and biomechanical constraints. We further explored if coordination and stability between the arms deteriorate when the legs are added to the task. A decrease in both measures was expected in children with USCP and TDC due to increased task difficulty. The second aim of this study was to determine if HABIT and/or CIMT could improve continuous inter-limb coordination and stability in children with USCP. We hypothesized that both parameters would improve between the arms and between the more-affected arm and leg post-intervention.
Section snippets
Participants
Children with USCP were recruited from a convenience sample at Teachers College as part of an ongoing trial (ClinicalTrials.gov, CT00305006). The experimental protocol was approved by the Teachers College, Columbia University Institutional Review Board and caregivers provided informed consent. Inclusion criteria were 1) lift the more-affected arm 15cm above a table and grasp light objects 2) >50% difference in the Jebsen-Taylor Test of Hand Function (JTTHF) between hands and more-affected hand
Participant Characteristics
There were no differences between groups in age, anthropometrics, or hand function (Table 1). Adherence to treatment was 100%.
Differences in coordination and stability between the arms in children with USCP and TDC during a standing with asymmetric arm swing task.
The USCP group demonstrated significantly less symmetrical arm swing (p<0.01) and longer mean cycle duration (p<0.01) compared to TDC during this task (Table 2). The amplitude (p<0.01) and variability (p<0.01) of the non-dominant arm swing of TDC were greater than the more-affected arm of children with USCP (Table 2). TDC demonstrated significantly higher MARP between
Discussion
The aims of this study were to evaluate continuous inter-limb coordination and stability in children with USCP compared to TDC, and to determine if coordination and stability in children with USCP improved after intensive upper extremity intervention of either HABIT or CIMT. In partial support of the hypothesis, children with USCP displayed a lower level of coordination compared to TDC, though stability did not differ. All children had greater difficulty coordinating their arms while marching
Conclusion
This study used a new approach to evaluate coordination and stability in children with USCP and TDC, in which continuous measures of relative phase were applied to continuous gross motor tasks. Previous research has attempted to understand bimanual coordination in these populations within the context of discrete tasks and spatiotemporal variables. This study’s approach was successful in determining the differences in coordination and between children with USCP and TDC and that these parameters
Acknowledgments:
The authors would like to acknowledge all children and families who participated in our study. Thanks to Dr. Richard Magill for providing his motor-learning expertise and Dr. Jaya Rachwani for her contribution of the Datavyu code. Also, thanks to Gregory Youdan and Avery Kratzer for their valuable technical assistance.
Declaration of Competing Interest
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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