Cerebral palsy (CP) is described as a group of permanent disorders of the development of movement and posture attributed to nonprogressive injury or abnormal development occurring in the fetal or infant brain.1 As a result of the injury/disturbance, children with CP typically present with primary and secondary impairments of body function and structure.2Primary impairments are problems that are apparent at the time of diagnosis, and secondary impairments are problems that occur over time, often as the result of primary impairments.3 For children with CP, common primary impairments include aberrations in muscle tone, postural stability, and motor coordination. These are considered primary impairments because they are the direct result of the injury/disturbance that occurred in the developing brain. Over time, many children with CP will develop secondary impairments such as decreased range of motion, force production, and endurance. Although decreased force production is a primary impairment associated with CP, we have conceptualized this construct as a secondary impairment because of the known secondary changes over time.4 These secondary impairments are potentially preventable and with intervention may improve the motor and participation outcomes of young children with CP. The ability to accurately measure primary and secondary impairments in young children with CP is important as it allows the therapist to monitor the effect of primary impairments and the progression of secondary impairments. The periodic measurement of primary and secondary impairments in young children should assist in understanding development and allow therapists to focus interventions to lessen the effect of the impairments.
Children with CP present with a wide range of motor ability levels. The Gross Motor Function Classification System (GMFCS)5 outlines this range of abilities, with classifications of level I “walks without restrictions” to level V “transported in a manual wheelchair.” Primary and secondary impairments are associated with a child's ability to attain motor function3,6; therefore, differences in the presence and severity of primary and secondary impairments should be evident across GMFCS levels.
The greatest increase in gross motor development in children with CP occurs between 1½ to 5 years of age7; accordingly, it is of interest to understand developmental changes in impairments in preschool-aged children with CP. With respect to primary impairments, in a retrospective analysis, Hägglund and Wagner8 reported that Modified Ashworth Scale (MAS) scores for muscle tone of the gastrocnemius-soleus in children with CP increase up to 4 years of age and then decrease to 12 years of age. Information on sex differences in muscle tone is lacking. Although motor incoordination is a hallmark of the CP diagnosis, no studies have examined motor coordination development in children with CP.
Postural stability typically continues to develop over the first 6 years of life9,10; this development is slower for children with CP.9,10 Using the Early Clinical Assessment of Balance, children with CP younger than 31 months have demonstrated lower median postural stability scores than children 31 to 60 months of age, indicating potential postural stability development in this population.9 No significant differences in postural stability have been reported between boys and girls.10
Little information on developmental differences in secondary impairments for young children with CP is available. Changes in lower extremity range of motion with age have been noted in children that are typically developing, but these differences are generally very minor, representing less than 5° to 8°, from 18 months to 5 years of age.11 To our knowledge, information specific to age-related changes in range of motion for young children with CP is not currently available. Although it seems reasonable to assume that as children age their strength increases with repeated practice of motor tasks, limited information is available describing differences in strength for children with typical development under 4 years of age. This may be due, in part, to difficulties with reliability of testing procedures in young children.12 Finally, in our current research using the Early Activity Scale for Endurance, significant differences in endurance for activity across ages have not been found for young children with CP.13 Sex differences among youth with CP have been noted after puberty, especially in the areas of range of motion,10 strength,14 and endurance,15 but have not been shown in young children.
The purposes of this study were to (1) describe the distribution of primary and secondary impairments in young children with CP under the age of 5 years across GMFCS levels and age and sex groups; (2) determine whether differences exist in primary and secondary impairments on the basis of GMFCS, age, or sex; and 3) explore the extent to which individual impairments accounted for the larger constructs of primary and secondary impairments.
This descriptive study is part of a prospective multisite study, entitled Movement and Participation in Life Activities of Young Children With Cerebral Palsy (Move & PLAY), which aimed to understand the child, family, and service delivery determinants that together explain the motor abilities, self-care, and play of young children with CP.4,16 This study was reviewed and received ethics approval from Institutional Review Boards at all participating institutions. All parents or guardians provided informed consent.
A convenience sample of 429 children with CP from 6 provinces across Canada (British Columbia, Saskatchewan, Manitoba, Ontario, Nova Scotia, and Newfoundland and Labrador) and 4 regions across the United States (Greater Seattle, WA; Greater Philadelphia, PA; Greater Oklahoma City, OK; and Greater Atlanta, GA) participated in this study. Parents provided demographic information on themselves and their children. Children were 18 to 60 months of age (mean = 38.0; standard deviation = 11) and 242 (56%) were boys. Children were placed in 3 age groups—18 to 30 months, 31 to 42 months, or 43 to 60 months—to divide the sample into children who were approximately 2, 3, and 4 years of age, respectively. The children represented all levels of the GMFCS, and distribution of GMFCS levels was representative of population-based studies.17 Therapists, who served as study assessors, classified the child's distribution of involvement into 1 of the 5 categories: monoplegia, hemiplegia, diplegia, triplegia, or quadriplegia (Figure 1). Table 1 summarizes the characteristics of the child and parent participants.
Gross Motor Function Classification System
The GMFCS4 is a 5-level classification system of gross motor function including the child's performance in sitting, transfers, walking, and wheeled mobility designed for children with CP. Distinctions between levels of the GMFCS are based on the need for assistive devices and caregiver assistance. The 2- to 4-year and 4- to 6-year-old age bands were used for this study. For 18- to 23-month-old children, the 2- to 4-year-old age band was used (and confirmed when children were older than 2 years). Research has supported content validity, construct validity, and inter-rater reliability of the GMFCS.7,18
Primary Impairment Measures
Modified Ashworth Scale
The Modified Ashworth Scale (MAS) is a measure of muscle tone performed by passively moving a joint through the available range of motion and scoring the perceived resistance to movement on a scale of 1 (no increase in tone) to 5 (affected part(s) rigid in flexion or extension).19 Reliability of the MAS has ranged from poor19 to good,19,20 depending on the muscle group tested for children with CP. Clopton and colleagues19 noted good reliability only for the elbow flexors and hamstrings with the MAS. For this study, trained raters measured muscle tone for elbow flexors and hamstrings bilaterally, 3 trials each. The variable used in analyses was the average of the first measurements for both elbow flexors and hamstrings, as each trial was highly correlated with the first measurement, providing evidence for intra-rater reliability in our study.
Early Clinical Assessment of Balance
The Early Clinical Assessment of Balance (ECAB) is a 13-item test that estimates postural stability for children with CP across all levels of functional ability.10 Details of test construction, items, and support for construct and concurrent validity in young children with CP who were participants in the Move & PLAY study (n = 410) can be found elsewhere.10 Excellent inter-rater reliability, test-retest reliability, and construct validity have been verified in a smaller group of 28 children who were 2 to 7 years old and from all GMFCS functional ability levels.21
Gross Motor Performance Measure
The Gross Motor Performance Measure (GMPM) is an evaluative measure of the quality of gross motor behavior for children with CP.22 The GMPM consists of 20 items designed to assess alignment, coordination, dissociated movement, stability, and weight shift in gross motor performance. Excellent interrater (intraclass correlation coefficient [ICC] = 0.93), intrarater (ICC = 0.92), and test-retest reliability (ICC = 0.96) of the GMPM have been reported.23 In this study, we examined 2 attributes of this measure: coordination and dissociated movement. The GMPM is used in conjunction with the Gross Motor Function Measure (GMFM),24 in that GMPM ratings (from 0 meaning “severely abnormal” to 3 meaning “normal”) are completed on items within the GMFM. GMPM ratings for both selected attributes were made for 3 trials of 2 GMFM items within the child's current motor repertoire. The average of the trials for each attribute was calculated, and the 2 attribute scores were summed for a possible range of values from 0 to 6.
Secondary Impairment Measures
Spinal Alignment and Range of Motion Measure
The Spinal Alignment and Range of Motion Measure (SAROMM) is a measure of spinal alignment and range of motion using standard physical therapy techniques scored on a 5-point ordinal score of 0 (normal alignment and range with active correction) to 4 (“severe” fixed deformity).25 The SAROMM has good reliability and validity for use with children with CP.26 The average of all item scores was calculated and recorded for each child. This measure can be accessed at www.canchild.ca/en/measures/saromm.asp.
Functional Strength Assessment
Therapists completed a functional strength assessment (FSA) to obtain an estimate of strength for major muscle groups including the neck and trunk flexors and extensors, and hip extensors, knee extensors, and shoulder flexors bilaterally. Scoring options were 1 (only flicker of contraction or just initiate movement against gravity), 2 (unable to move completely against gravity), 3 (full available range against gravity but no resistance), 4 (full available range against gravity and some resistance), and 5 (full available range against gravity and strong resistance). Multiple testing trials per muscle group were allowed on the basis of therapists' judgment for obtaining best performance, with therapists then selecting 1 rating to describe each muscle group. The mean of all the muscle group test scores was used for analysis. During data collection on 28 Move & PLAY participants, 1 study rater administered and scored the test and then a second study rater or investigator who was observing the first measurement repeated the measure and scored. Interrater reliability was found to be high, ICC (2,1) = 0.996 (95% confidence interval = 0.991-0.998), P < .001. Construct validity is supported by similarity of this pragmatic approach to testing groups of muscles to standard manual testing of individual muscles typically used by physical therapists. This measure can be accessed at www.canchild.ca/en/ourresearch/resources/MuscleStrength.pdf.
Early Activity Scale for Endurance
Endurance for activity for this study was measured using a 4-item version of a parent-completed questionnaire, the Early Activity Scale for Endurance (EASE).13 The 4-item EASE was determined through confirmatory factor analysis of the original 11-item questionnaire created by the Move & PLAY investigators on 427 Move & PLAY participants. The 4-item EASE was found to report appropriately on endurance for activity (χ2 = 2.8, P > .05; comparative fit index = 0.998; Tucker-Lewis index = 0.993; root mean square error of approximation = 0.03). Ratings made by parents are on a scale of 1 to 5 (1 = never; 5 = always), with higher scores indicating greater endurance for activity. The final score is a mean of all item scores. The shorter version correlates well with the full-length version (Pearson r = 0.88; P < .001).13 Validity of the EASE 4-item scale is also supported by moderate correlations (Spearman r = 0.41; P = .01) with the 6-Minute Walk Test in a group of 35 children age 3 to 6 years composed of 21 children without CP and 14 with CP at GMFCS levels I or II. Test-retest reliability (parents completed the EASE twice within a mean of 25.7 days [standard deviation = 18.4]) for 32 children was found to be acceptable, ICC (2,1) = 0.79 (95% confidence interval = 0.62-0.89).
Move & PLAY assessors participated in training at multiple sites, which included presentations and video analysis. Assessors completed criterion testing from criterion videos (ie, “reference standard” scores were established by 2 or more investigators through consensus and used as criterion standards) after training and before data collection. A baseline of 80% agreement was required. The percent agreement achieved by the 61 assessors were GMFCS (>80% agreement achieved by all on the day of training), ECAB (90.8% and 91.4% on 2 individual measures that were transformed into the ECAB9), GMPM (92.1%), and SAROMM (88.9). Standardized procedures were used to train all assessors in the MAS and FSA measurement methods, but no criterion checks were completed because of the nature of having to handle the child to make measurement judgments.
At the initial assessment session of the Move & Play study, parents completed a booklet that included the EASE and the demographic forms. Assessors completed all other measures in the following order GMFM, GMPM, ECAB, FSA, SAROMM, MAS, distribution, and GMFCS taking into account the child's tolerance and providing breaks as needed. The testing session took between 1 and 1.5 hours in the family home or a clinic setting.
Data were analyzed using the Statistical Package for Social Sciences (Version 18). Descriptive statistics on the primary impairments (MAS and GMPM) and secondary impairments (SAROMM, FSA, and EASE) were completed, and skewness for each variable was examined. All variables demonstrated normal distributions; therefore, parametric statistics were used. Comparisons among GMFCS levels and age groups were completed using a 1-way analysis of variance, with Scheffé post-hoc follow-up tests for pairwise comparisons; t tests were used for comparison across sex groups. (Descriptive and comparative analyses of the ECAB scores can be found in McCoy et al.9) An alpha level of .05 was used to indicate significance for overall testing. Factor loading was examined using confirmatory factor analysis to indicate the extent to which each factor loaded into the primary or secondary impairment construct.
Results for all variables can be found in Table 2 (descriptives) and Table 3 (comparisons) and Figures 2 and 3. The mean MAS score ranged from 1.5 to 3.5 for children in GMFCS levels I and V, respectively. Differences in the MAS were found across all GMFCS levels (P < .001), except for the comparison of children in GMFCS levels II versus III. The mean GMPM (coordination/dissociated movement) score ranged from 3.93 to 0.13 for children in GMFCS levels I and V, respectively. GMPM scores differed across all GMFCS levels (P < .001), except for the comparison of children in GMFCS levels I versus II. The mean SAROMM score ranged from 0.34 to 1.46 for children in GMFCS levels I and V, respectively. The children's spinal alignment and peripheral joint motion differed across all GMFCS levels (P < .001), except for the comparison of children in GMFCS levels II versus III. The mean FSA score ranged from 4.41 to 2.23 in children at GMFCS levels I and V, respectively. Differences in FSA were found across all GMFCS levels (P < .001), except for the comparison of children in GMFCS levels II to III. The mean EASE 4-item score ranged from 3.90 to 1.88 in children at GMFCS levels I and V, respectively. Differences in EASE 4-item scores were found between GMFCS levels I and V when compared with all other levels (P < .002). No statistically significant differences were found between children at GMFCS levels II versus III, II versus IV, or III versus IV.
Age and Sex Comparisons
No differences were identified for any of the variables on the basis of the age groups (18-30 months, 31-42 months, or 43-60 months) or sex (Table 3).
Factor Loading Analyses
The indicators for primary impairments demonstrated a good fit with the construct (χ2 = 0; df (1); P = .991, with all fit indices = 1), demonstrating that postural stability (ECAB), distribution of involvement, muscle tone (MAS), and coordination/dissociation (GMPM) all contributed to the construct of primary impairments. The factor loadings for individual impairments were postural stability 0.95, distribution 0.82, coordination 0.77, and muscle tone 0.68. Factor loadings for secondary impairments demonstrated a perfect fit, so no χ2 was calculated, demonstrating that range of motion (SAROMM), strength (FSA), and endurance for activity (EASE) all contributed to the construct of secondary impairments. The factor loadings for individual impairments were muscle strength 0.95, range of motion 0.74, and endurance for activity 0.66.
The primary aim of this article was to describe the distribution of primary and secondary impairments across the full functional spectrum of young children with CP using clinically feasible measures. Results of this study indicate that young children with CP present with primary impairments in distribution of involvement, muscle tone, and quality of movement, as was expected. Children with CP, even at a preschool age, also present with secondary impairments in range of motion, strength, and endurance. Of particular note, even young children at a GMFCS level I showed secondary impairments. These findings are similar to previous research by Ostensjo et al,26 who examined primary and secondary impairments in a smaller sample of older children with CP, up to 7½ years of age.
We identified differences in primary and secondary impairments among GMFCS levels with an increasing degree of impairment noted as the children's GMFCS level increased. This is not surprising, but it provides validation to a common assumption that more limiting primary and secondary impairments are seen in children with greater functional limitations.
Significant differences among GMFCS levels, however, varied on the basis of the particular impairment. For primary impairment scores, the MAS was not different between children in GMFCS levels II and III, and GMPM (coordination/dissociated movement) was not different between children in GMFCS levels I and II. All secondary impairments did not differ for children in GMFCS levels II and III. The EASE scores for children at GMFCS levels II to IV did not differ.
The lack of differences between children in GMFCS levels II and III could be related to the movement development that determines the GMFCS classification of children at this young age. Children in GMFCS levels II and III before age 4 years typically present with creeping or crawling as their primary means of mobility, and when standing they continue to rely on supports for mobility—from an assistive device, furniture, or caregiver.5 As children move into the 4- to 6-year-old GMFCS age band, gross motor upright mobility differentiates with children in GMFCS level II gaining gross motor control without an assistive device and children at GMFCS level III continuing to require support. At this older age to have upright mobility without an assistive device, subtle differences may exist that we did not capture in our measures of their strength and postural stability and potentially, their range of motion. Examination of primary and secondary impairments in older children in GMFCS levels II and III would be interesting to determine whether, as children in these levels age, differences in impairments are noted. This may help determine where to focus intervention strategies for children with CP as they age. The similarity of children in GMFCS levels I and II on the GMPM (coordination/dissociated movement) could be related to the tool's sensitivity to differences in coordination and disassociation of movements, because children in these levels present with higher-level motor function. Lack of differences between levels II, III, and IV on the EASE may also be related to the sensitivity of the EASE, as it is a parent questionnaire that serves as a proxy for endurance for activity. Further investigation with a larger population and longitudinally tracking children's primary and secondary impairments is needed to provide clarity on the differences in primary and secondary impairments at these GMFCS levels.
No differences related to age were noted in primary or secondary impairments in this group of young children with CP. When postural stability was examined using the ECAB, there was a difference noted, with children younger than 31 months demonstrating lower postural stability scores than the older children.10
No differences related to sex were noted in primary or secondary impairments in this group of young children with CP. The lack of sex-based differences on the MAS differs from findings in a longitudinal study by Hägglund and Wagner,8 which indicated increases in the MAS as children aged from birth to 4 years. This discrepancy could be related to the way in which the MAS was used within each study; our MAS measurement included evaluation of the elbow and knee flexor muscles bilaterally, yielding an overall mean summary score, whereas Hägglund and Wagner8 measured the gastrocnemius-soleus muscles.
Endurance for activity on the EASE did not reach the statistical significance set for our study. The EASE score difference between boys and girls was small (mean difference = 0.22; standard error of difference = 0.11, representing ∼5% of the scale range), this difference is not thought to be clinically meaningful in this age group. Nonetheless, differences in endurance for activity may become apparent as children age, which has been noted in research examining older children with CP.27
Examination of our construct of primary impairments using our measures of muscle tone, postural stability, and coordination showed that all contributed to the construct; however, postural stability had the highest factor loading. Previous research has suggested that postural stability is amenable to change,9 and, due to its importance in the factor loading, we suggest that it should be an integral aspect of intervention programs for young children with CP. Examination of our construct of secondary impairments using our measures revealed that strength, range of motion, and endurance all contributed to the construct, with strength having the highest factor loading. Similar to postural stability, muscle strength has been found to be amenable to change.28 Research suggests, however, that impairment intervention is more effective at improving function when performed within functional activities.29
A limitation of this study is lack of obtaining inter-rater reliability before the assessors' use of the MAS and FSA impairment measures. However, during the study researchers obtained subsequent support for intrarater reliability on the MAS and interrater reliability of the FSA.
CONCLUSIONS AND FUTURE WORK
This study demonstrates the use of an easily administered set of examination tools for monitoring impairments in young children with CP. Although young children with CP presenting with primary impairments related to their diagnosis is not new information, we show that they are already demonstrating secondary impairments, even those at GMFCS level I, as young as 18 to 30 months of age. Therapists should monitor children's primary and secondary impairments and consider preventive measures, especially focusing on postural stability and strengthening within functional activities. A study to monitor longitudinal change over time among preschool- and school-aged children is currently in progress (https://www.canchild.ca/en/ourresearch/on_track_study.asp), which we expect will elucidate changes with age over a broader period. On the basis of how children change across time, therapists should individualize interventions to support overall function and to help prevent future development of secondary impairments.
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Keywords:Copyright © 2016 Academy of Pediatric Physical Therapy of the American Physical Therapy Association
age factors; cerebral palsy/classification; cerebral palsy/prevention and control; child; muscle strength; muscle tone; physical endurance; physical therapy/methods; postural balance; posture; psychomotor performance; range of motion; sex factors