Children with cerebral palsy (CP) have impairments of body function and structure.1,2 Balance is considered a primary impairment since challenges in postural control in both static and dynamic activities are frequently present at the time of diagnosis.3–5 As children with CP age, secondary impairments often develop including restrictions in joint range of motion (ROM) and decreased endurance and strength.2,6,7 A primary goal of therapy is to monitor the development of impairments and focus intervention on the reduction of current impairments and prevention of further secondary impairments.
Researchers have documented impairments in children with CP at all functional motor ability levels of the Gross Motor Function Classification System (GMFCS)8 and as young as 18 months.2,6,9–11 However, most studies use cross-sectional methodology that provide results for a cohort of children at one point in time. Based on this cross-sectional data, children with CP have impairments and differ by GMFCS levels.2 A cross-sectional study provides valuable information but does not describe the development of the impairments over time.
The opportunity occurred to longitudinally examine children with CP who participated in 2 multisite, international, prospective studies.12,13 Using the same clinical measures, we examined changes in impairments in a group of children with CP following several years of development. The purposes of this study were to (1) determine whether a change occurs over time for impairments of balance (Early Clinical Assessment of Balance [ECAB]),14 ROM (Spinal Alignment and Range of Motion Measure [SAROMM]),15 endurance for activity (Early Activity Scale for Endurance [EASE]),16 and strength (Functional Strength Assessment [FSA])2 in children with CP.
This study examined results from the Movement and Participation in Life Activities of Young Children with Cerebral Palsy (Move & PLAY) and On Track: Monitoring Development of Children with Cerebral Palsy and Gross Motor Delay (On Track) studies. Move & PLAY aimed to understand the child, family, and service delivery determinants that together explained the motor abilities, self-care, and play of young children with CP.12,17 On Track aimed to create longitudinal developmental trajectories and reference percentiles for impairments, health conditions, and participation variables for children with CP.13 This current analysis includes children with CP who participated in both studies. Full study protocols have been reported.13,18 All participating institutions and recruitment sites with Institutional Review Boards (IRBs) provided ethics approval. Parents or guardians provided informed consent and children, as appropriate and in compliance with the specific IRB, provided assent for both studies.
A convenience sample of 77 children with CP participated in the studies, from 6 provinces in Canada, including British Columbia, Saskatchewan, Manitoba, Ontario, Nova Scotia, and Newfoundland, and 4 regions of the United States, including areas within and surrounding Georgia, Oklahoma, Pennsylvania, and Washington. Of this sample, 52% of the participants were from the United States. Participants were recruited through children's rehabilitation centers in Canada and through physical therapists, occupational therapists, physicians, and hospital systems in the United States. All children had a diagnosis of CP. Children were excluded if their parents were unable to speak and understand English, French, or Spanish.
Gross Motor Function Classification System
The GMFCS is a 5-point classification system used to describe gross motor function ability including sitting, transfers, walking, and wheeled mobility for children with CP. The child's functional abilities, use of assistive technology, and need for caregiver assistance differentiate the levels.8 The GMFCS levels are divided into age bands to clearly describe gross motor function. GMFCS content validity,8 construct validity, and interrater reliability have previously been supported.19–21
Early Clinical Assessment of Balance
The ECAB provides an estimate of postural stability for children with CP at all GMFCS levels.14 The assessor examines the child's head and trunk control, protective responses, upright posture in sitting and standing, and postural adjustments during voluntary movements in standing. The ECAB has known-group validity for children with CP 1.5 to 12 years of age, with average scores that differ between age groups and GMFCS levels (P < .001),14 and has excellent interrater (ICC (2,1) = 0.99) and test-retest (ICC (2,1) = 0.99) reliabilty.22 The ECAB has a minimal detectible change (MDC95) of 10 points.14 The total ECAB score out of 100 was used for analysis. The higher the score, the better the balance.
Spinal Alignment and Range of Motion Measure
The SAROMM provides an estimate of spinal alignment and ROM and muscle extensibility using standard physical therapy measurement techniques.15 The assessor scores 4 spinal alignment items using a 5-point ordinal score of 0 (“no alignment limitations with active correction”) to 4 (“fixed”—limitation is structural, static, not reducible and severe). For the remaining extremity ROM and muscle extensibility items, the assessor scores items using a 5-point ordinal score of 0 (“normal”—no restrictions of ROM on passive testing and no postures typical of some children with CP) to 4 (“fixed”—limitation is structural, static, irreducible and is severe); hence, a lower score is better ROM.15 Researchers report good validity, interrater reliability (ICC (2,1) = 0.89), and test-retest reliability (ICC (2,1) = 0.93) when used with children with CP.15 For the SAROMM total score, the MDC90 has been reported as 3.22,23 MDC95 as 9 points,15 and the minimal clinically important difference (MCID) is 4.53.23 The mean of item scores for each child was used for analysis.
Four-Item Early Activity Scale for Endurance
The 4-item EASE includes 4 questions of parent perception of the child's endurance for activity.16 Questions are scored using a 5-point ordinal scale of 1 (never) to 5 (always) and include the child's (1) physical activity related to peers, (2) physical energy level and their need to take breaks, (3) frequency of breathing quickly and getting flushed during activity, and (4) frequency of daily activities requiring a lot of physical energy. Higher scores indicate greater endurance for activity. The EASE is moderately correlated (Spearman r = 0.41, P = .01) with the Six-Minute Walk Test16 and has acceptable interrater reliability (ICC (2,1) = 0.79).16 The EASE does not have a calculated MDC. The mean EASE score was used for analysis.
Functional Strength Assessment
The FSA includes an assessment of movements against gravity and resistance, providing an estimate of the child's strength in major muscle groups.2 The assessor rates the child's strength using a 5-point ordinal scale ranging from 1 (only flicker of contraction or just initiates movement against gravity) to 5 (full available range against gravity and strong resistance) for major muscle groups (neck and trunk flexors and extensors, hip extensors, knee extensors, and shoulder flexors).2 The FSA has excellent interrater reliability (ICC (2,1) = 0.996)2; however, the FSA does not have a calculated MDC. The mean FSA score is used for analysis, with a higher score indicating better strength.
The ECAB, SAROMM, EASE, and FSA forms and training protocols can be accessed through the CanChild Web site (https://www.canchild.ca/en/research-in-practice/current-studies/on-track/on-track-measures).
Therapist assessors were physical therapists and occupational therapists, with at least 1 year of experience, from Canada and the United States, who completed on-site training prior to data collection. Therapists also completed videotaped criterion tests of the ECAB, SAROMM, and FSA measures and obtained 80% or greater item agreement, with the study investigators providing “gold standard” responses.
Data from the first assessment of the Move & PLAY study (T1), collected between summer 2007 and spring 2009, and data from the first assessment of the On Track study (T2), collected between spring 2013 and summer 2014, were used for this analysis. Parents completed the EASE and a demographic questionnaire. Therapist assessors completed the ECAB, SAROMM, and FSA. The parent and the therapist assessor independently completed the GMFCS and a consensus rating was determined.24 For this analysis, we used the GMFCS rating from the On Track study (T2) because some children at T1 were younger than 2 years and GMFCS reliability is greater after 2 years of age.19
Data were analyzed using the Statistical Package for Social Sciences (version 18). Descriptive statistics of participants are given in Table 1. Median and minimum/maximum ranges for impairments (ECAB, SAROMM, EASE, and FSA) are given in Table 2. Because of the small sample size of children at GMFCS level III, these children were combined with children at GMFCS level IV for group comparisons for the impairment measures. The Wilcoxon signed ranked test was used for comparison of medians between T1 and T2 for GMFCS level groups (Table 2). Comparisons of median scores for each variable across GMFCS level groups were completed for data at both T1 and T2 using nonparametric Kruskal-Wallis tests with post hoc pairwise comparisons to determine whether significant differences existed across GMFCS levels (Table 3). An α level of P < .05 was used for significance.
Participants were 1.5 to 4.6 years old (mean = 2.9 years, SD = 0.9) at T1 and 6.3 to 11.1 years old (mean = 8.7 years, SD =1.1) at T2 and 52% were males and 79% were white. The proportion of children in each GMFCS level in our sample was as follows: GMFCS I, 26.0% (N = 20); GMFCS II, 29.9% (N = 23); GMFCS III, 9.1% (N = 7); GMFCS IV, 13.0% (N = 10); and GMFCS V, 22.1% (N = 17). On average, the time difference between T1 and T2 was 5.8 years (SD = 0.6). Table 1 provides demographic information.
Comparing ECAB scores over time, significant improvements in balance were noted for children in GMFCS levels I (P < .001), II (P < .001), and III/IV (P = .008) (Table 2). At both T1 and T2 assessments, significant differences were noted on the ECAB across all comparisons, with children with more functional mobility demonstrating higher ECAB scores than children with less functional mobility (Table 3).
Over time, SAROMM scores were significantly higher at T2 for children in GMFCS levels III/IV (P = .005) and V (P < .001), indicating greater ROM restrictions (Table 2). At both T1 and T2 assessments, there were significant differences on the SAROMM scores across all comparisons, except between children in levels II and III/IV at T1 (Table 3).
There were no differences in EASE scores within GMFCS levels over time (Table 2). On the EASE, at both T1 and T2 assessments, there were significant differences across all comparisons, except between children in levels II and III/IV at both T1 and T2 (Table 3).
There were significant improvements in strength for children in GMFCS levels I (P < .001) and II (P < .001) (Table 2). At both T1 and T2 assessments, there were significant differences on the FSA in all comparisons, except between children in levels II and III/IV at T1 and between children in levels I and II at T2 (Table 3).
We longitudinally followed 77 children with CP over a multiyear period to explore how commonly identified impairments changed over time. Finding for each construct are discussed as follows:
Significant differences in balance were noted from T1 to T2 for all children with CP except those with GMFCS level V. As expected, children with more gross motor ability demonstrated better balance than children with less gross motor ability. For the majority of children, the amount of change in balance was greater than the minimal amount of change required to differentiate a true change versus a change due to variability in performance.
As balance is correlated with gross motor ability25 and gross motor skills continue to develop as children with CP age,26 this improvement was expected. For children in level V, the balance median score decreased. Gross motor skills of children at level V plateau on average at 2 years 7 months,18 indicating that gross motor skills are not changing; therefore, balance skills will not change. This longitudinal exploration of balance in children with CP provides a beginning analysis. Continued exploration is needed to determine whether differences in service focus and frequency influence a child's balance abilities.
Similar to the results of Ostensjo and colleagues,9 children with CP in our study presented with some degree of ROM and spinal alignment restrictions regardless of GMFCS levels. As expected, children with higher functional mobility had fewer restrictions than children with lower functional abilities. For the majority of children, the amount of change in ROM scores was greater than the minimal amount of change required to differentiate a true change and they had restrictions beyond what is typically considered a clinical change that influences their daily activities.
When ROM and spinal alignment were measured over time, children at GMFCS levels I and II did not have a significant change. Direct correlations cannot be examined to determine what prevented the progression of joint restrictions; however, we can hypothesize that independent mobility likely facilitates joint and spinal flexibility. Children with higher GMFCS levels rely on assistive devices for mobility (walkers or wheelchairs) and spend increased time seated or lying down; therefore, these static postures likely contribute to the development of secondary impairments in ROM. This presents as an opportune window for intervention to prevent increases in joint restrictions, particularly for children at levels III to V. The challenge is to identify what intervention should be used. Based on a systematic review, brief stretching has little to no effect either in the short term or in the long term on improving joint mobility in persons with neurological conditions.27 A heightened focus on increasing targeted functional activities and more frequent changes in positions for those at GMFCS level V may prevent further ROM restrictions. We do not know the details of interventions to prevent secondary impairments and how increasing environmental modifications may alter the development of ROM restrictions.
As we expected, endurance for activity was higher for children with higher functional mobility. Median EASE scores decreased at each GMFCS level but were not significantly different over time. What is unknown is whether endurance is relatively constant over time for children with CP in this age range, the tool is not sensitive enough for longitudinal change, or a larger sample of children is needed to identify longitudinal change. We know from physical activity literature that endurance typically decreases in adolescents without disabilities.28 Following children with CP is needed to identify whether and when changes in endurance occur.
Since parents report no change in endurance, we hypothesize that this is not a focused area of intervention. We recommend that therapists consider targeted interventions focused on endurance at all GMFCS levels and ages.
As expected, strength scores were higher for children with higher motor function. Over time, strength scores significantly improved for children in GMFCS levels I and II. This is congruent with literature demonstrating that children with CP have the ability to strengthen various muscle groups.29 In addition, the FSA scores for children in the other GMFCS levels increased but were not significantly different across time. There are varying results in the literature related to strengthening interventions for children with CP and the carry over to functional motor skills.30 Most literature focuses on children at GMFCS levels I to III since they more often have the ability to demonstrate selective motor control. Given that a focus on services related to secondary impairments increases over time, more details from therapists would be helpful to determine effective strengthening interventions especially for children with lower functional ability.
As most children with CP receive therapy services during early childhood, therapists have the opportunity to support maturation during this critical period of growth and skill development. Although we were unable to determine the effect of therapy services or the child's natural evolution of skill mastery, most children with CP were stronger, had better balance, and their endurance had not significantly declined after almost 6 years. Based on these results and the knowledge that in adolescents and young adulthood, individuals get heavier and flexibility and endurance decline,28,31,32 therapists should encourage health and wellness programs that focus on strength and cardiopulmonary fitness whether that be in a therapist-directed or community program.
The primary limitation of this study is the small sample size. To acknowledge this, we used nonparametric statistics for data analysis. We did not correct for multiple analyses; however, as most P values were below .001, one could determine this was not a problem. We also combined data for children in GMFCS levels III and IV. The EASE and FSA measures do not have MDC or MCID values, which would have provided additional information regarding change over time. This study had a slightly lower proportion of children at GMFCS level I and a greater proportion of children at level V compared with the Reid and colleagues33 determination of the GMFCS distribution of CP based on multiple international registries. Finally, a potential sampling bias could be present as parents agreed to participate in 2 research studies over time, which could indicate they are closely linked to rehabilitation providers and potentially engaged in intervention programs more than other children.
The results of this study indicate there are improvements in children with CP within some impairment areas (balance and strength); however, greater ROM restrictions and no changes in endurance are noted over an extended time period. These changes support the need for physical therapists to monitor and focus interventions on primary and secondary impairments in children with CP, given the hypothesis that each of these impairments can potentially impact the children's ability to perform daily activities and participate in home, school, and community environments. Based on this longitudinal study, continued monitoring of impairments and collaboration with families is important for the development of children with CP.
The authors acknowledge additional Move & PLAY and On Track Study Team members including academic researchers: Doreen Bartlett, Lisa Chiarello, Robert Palisano, Pitor Wilk, Peter Rosenbaum, and Jan Willem Gorter; Canadian project coordinator Barb Galuppi; US project coordinator Monica Smersh; and parent researchers, Lisa Diller, Paula Drew, Nancy Ford, Marquitha Gilbert, Tina Hjorngaard, Kimberly Rayfield, and Barbara Sieck Taylor.
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