INTRODUCTION AND PURPOSE
Cerebral palsy (CP) is the result of a nonprogressive brain injury that occurs at or near the time of birth.1 CP is the most common cause of motor impairment among infants, affecting 1.4 to 3.1 in 1000 live births.2,3 Dependent on the size, type, timing, and location of the brain injury, impairments in movement and posture vary in severity and distribution.1 Historically, the first 1 to 2 years of life were considered a latent period, during which accurate CP diagnosis was not possible.4 This resulted in a “wait and see” approach to CP diagnosis, leading to a delay in referral to rehabilitation services to address activity and participation limitations.4 Published guidelines using a combination of imaging and standardized motor assessments, including the General Movement Assessment and the Hammersmith Infant Neurological Examination, for early diagnosis of CP or high risk of CP are now available.5 These diagnosis guidelines have been implemented in our institution since 2017.6 Infants with moderate to severe motor impairments are more likely to be diagnosed earlier because of medical history or because delays in typical developmental milestones may be noticed earlier.7
There are significant benefits to diagnosing CP at younger ages. One benefit is that early diagnosis allows for earlier referral to CP-specific intervention services like physical therapy.5 Movement experiences in infancy require activity-dependent stimulation of the corticospinal tracts.8 In typical development, neuromuscular connections that are used by developing infants are strengthened and maintained, while unused or inappropriate connections are pruned away. Injury to the cerebral cortex disrupts the typical activation patterns of neuronal networks, and can result in significant motor impairments, including weakness or paresis, decreased coordination, hyperreflexia or spasticity, and learned nonuse.8 There is growing evidence for early, motor learning-based rehabilitation for infants with CP.9 Specifically, intervention promoting task-specific, goal-directed, active movement is associated with better outcomes for infants with CP.9 Early CP diagnosis is an opportunity to initiate CP-specific rehabilitation that could maximize the plasticity of the developing neural system. Accurate evaluation of motor skills is a foundation for goal setting, so is critical to effective intervention planning.
Patient-reported outcome measures (PROMs) are a means to involve parents in the motor evaluation of their child. Human development occurs within the context of meaningful relationships, and the people with the greatest influence on developmental outcomes are those closest to the child, specifically parents.10 Parent empowerment and parent-therapist collaboration promotes the success of rehabilitative interventions because the plan of care can be based on goals meaningful to the child and family.11 PROMs provide accurate information about the daily motor performance of children with CP because (1) parents accurately report their child's motor function12,13; and (2) PROMs allow parents to provide information about typical daily function rather than best performance observed in a clinical setting.14 Intervention to address rehabilitation goals that are meaningful in the context of a family and based on typical daily function is more likely to promote improvements in a child's participation.15,16
The tests or measures used determine the information gained from a motor evaluation. The Gross Motor Function Classification System (GMFCS) is a stable descriptive classification scale of overall motor function for infants with CP.17 The GMFCS is useful for overall prognosis and treatment planning, but it is not an outcome measure, nor does it measure change in motor activities over time or in response to intervention. The Gross Motor Function Measure (GMFM) is a valid and reliable evaluation tool for measuring a child's capacity, or best performance, at the activity level of the International Classification of Functioning, Disability, and Health.18,19 In addition to capacity, typical performance in a daily context must be measured, as this determines how infants are using their motor skills to participate in meaningful activities with their families.16,18 The Pediatric Evaluation of Disability Index (PEDI) is a PROM of activities performed in typical daily life.20 The mobility domain of both the original and the computer-adapted versions of the PEDI (PEDI-CAT) has strong relationships with the GMFM among children older than 2 years across all GMFCS levels.13,18 This relationship has not yet been determined for infants with or at high risk for CP with more severe motor limitations.
With diagnostic practices allowing accurate identification of infants with CP or at high risk for CP, clinicians must use accurate motor assessment tools to establish baseline function and develop a plan of care. The purpose of this study is to determine (1) the relationship between a therapist-administered GMFM and parent-reported PEDI-CAT mobility domain (PEDI-mob) score; and (2) the relationship between PEDI-mob scores and GMFCS level for infants with CP or at high risk for CP. We hypothesize a direct relationship between GMFM scores and parent-reported PEDI-mob scores. We further hypothesize that parent-reported PEDI-mob scores will have an inverse relationship to GMFCS level.
This is a prospective, cohort study design. Some infants in this study participated in an intervention clinical trial (ClincalTrials.gov identifier: NCT02857933). Additional details of the primary trial have been described in a published protocol.21 The study was approved by The Ohio State University and Nationwide Children's Hospital's Institutional Review Boards. Infants were recruited between April 2016 and January 2020 from hospital-based developmental follow-up clinics and through word of mouth.
Fifty-four participants completed preintervention assessments during the recruitment period and were included in this study. Participants were eligible for the primary trial if they were between 6 and 24 months of age and had a diagnosis of CP or high risk for CP or moderate to severe motor delay equivalent to GMFCS levels III, IV, or V. Exclusion criteria were uncontrolled seizures, any comorbid condition or auditory or visual conditions that prevented full participation in treatment sessions; participation in a daily treatment program 6 months prior to the study; and progressive neurological disorders with no potential for improvement. Informed consent was provided via verbal and written consent by parents or legal guardians. A summary of the participants' age, sex, and level of gross motor function is shown in the Table.
||Total (N = 54)
|III (n = 24)
||IV (n = 21)
||V (n = 9)
|Age, mean (SD), mo
|Confirmed CP diagnosisb
|Distribution of involvementc
|Type of CPc
Abbreviations: CP, cerebral palsy; GMFCS, Gross Motor Function Classification System.
bConfirmed CP diagnosis at age 2 years.
cProportions based only on children with confirmed CP diagnosis at age 2 years.
Gross Motor Function Measure. The GMFM is a criterion-referenced, valid, and reliable standardized assessment tool that measures change in gross motor function over time or following an intervention among children with CP.22–24 It is considered the gold standard for evaluation of gross motor skills for children with CP.22 The GMFM-88 is a version of the GMFM with 88 items in 5 dimensions: (a) lying and rolling; (b) sitting; (c) crawling and kneeling; (d) standing; and (e) walking, running, and jumping.23,24 The GMFM-88 includes basic floor mobility skills and was selected over abbreviated versions of the GMFM because the participants for this study were young and had more significant motor impairment. Administration of the GMFM-88 requires 45 to 60 minutes.19
Pediatric Evaluation of Disability Index-Computer-Adapted Test. The PEDI-CAT is a revised version of the PEDI used for children from birth to 21 years old with a physical, behavioral, and/or cognitive condition. The PEDI-CAT has strong psychometric properties, and the PEDI-CAT mobility domain (PEDI-mob) has been validated with the mobility scale of the original PEDI.25,26 The PEDI-CAT assesses functional abilities across 4 domains: daily activities, mobility, social/cognitive, and responsibility. PEDI-mob scores were used for this analysis. PEDI-mob items focus on functional skills such as transfers, standing, walking, stair climbing, and running. This domain accounts for any mobility device the participant may use, such as canes, walkers, and wheelchairs. Using item response theory, parents or caregivers respond only to the most pertinent items for their child, so the PEDI-mob can be completed in as few as 4 minutes.27
Gross Motor Function Classification System. The GMFCS, a descriptive classification scale of overall motor function for children with CP, ranges from level I (independent function) to level V (total dependence on caregivers for mobility).17 Children classified as GMFCS level III, IV, or V have moderate to severe motor impairments.
Measures for this study were administered either in the home or in a home-like research laboratory environment and prior to the start of intervention. For those infants without a CP diagnosis when enrolled in this study, a diagnosis of CP was confirmed at age 2 via medical chart review. Study physical therapists completed all 5 dimensions of the GMFM-88 with each participant. Study therapists received GMFM-88 training and then completed intra- and interrater reliability testing. To establish reliability, blinded evaluators used video review to score selected GMFM-88 administrations with children. A senior study therapist served as the gold standard for scoring these recordings. For each blinded evaluator, the interrater correlation coefficient was calculated by dividing the number of items (88) by the number of item disagreements from the gold standard. All therapists needed to achieve and maintain 85% or more to pass reliability. After reliability was calculated, study therapists met to review questions and concerns on specific GMFM items. To maintain reliability, this process was completed for all study therapists every 6 months using approximately 10% of the assessments completed in the study. A parent or caregiver completed the PEDI-CAT on a tablet on the same day of GMFM-88 administration. Study therapists recorded the GMFCS level after GMFM-88 administration and confirmed the assigned level with the electronic medical record.
For descriptive statistics, means and standard deviations were calculated for age. Proportions were calculated for categorical data, including sex, race, confirmed CP diagnosis by age 2, distribution of impairments, and type of CP. Pearson's correlation coefficient was calculated to evaluate the strength of the relationship between the GMFM-88 Total Score and PEDI-mob scores. PEDI-mob scores across GMFCS levels were evaluated using analysis of variance. Post hoc pairwise comparisons between patients with different GMFCS levels were conducted with multiple comparison adjustment for P values. Data analysis was performed using Minitab Version 18.1 (Minitab, Inc). Significance level was set at an α level of P < .05.
Average age was 16.7 ± 4.6 months, and 30 infants (56%) were male. Infants were described by the following racial categories: 35 (64.8%) White, 9 (16.7%) Black or African American, 2 (3.7%) Asian, and 8 (14.8%) bi- or multiracial. Participant characteristics, grouped by their GMFCS levels, are shown in the Table. Looking at the overall sample prior to confirmation of CP diagnosis, 24 were classified as GMFCS level III (44%), 21 as level IV (39%), and 9 as level V (17%). Thirty-eight of the 54 infants (70%) had a diagnosis of CP when they were tested at baseline. Follow-up medical chart review at age 2 years confirmed the original 38 CP diagnoses and added 6 additional participants with a CP diagnosis, meaning that 11% of the sample had a “delayed” diagnosis. By age 2, at least 81% of our sample size had a confirmed CP diagnosis, with confirmed cases classified as GMFCS level III (n = 17, 31.5%), level IV (n = 20, 37.0%), or level V (n = 7, 13.0%). The remaining 10 children (18.5%) did not receive a CP diagnosis during or after the study. The majority of infants (n = 31, 70%) had an impairment distribution of quadriplegia, with greater variability of distribution for infants classified as GMFCS level III when compared with levels IV or V.
Relationship Between PEDI-mob and GMFM Total Score
The associations between the PEDI-mob scores and GMFM Total Scores are graphed in Figure 1. There was a significant correlation between PEDI-mob scores and GMFM Total Scores (r = 0.760, P < .001, 95% CI 0.62-0.85, P < .001).
Relationship Between PEDI-mob and GMFCS Levels
PEDI-mob scores varied across GMFCS levels (F(2,20) = 17.3, P < .0005). Mean PEDI-mob scores and 95% confidence intervals were 47.1 (45.3-48.9), 40.6 (37.6-43.5), and 35.0 (30.1-39.9) for infants with GMFCS levels III, IV, and V, respectively (Figure 2). Infants with higher GMFCS level had lower PEDI-mob scores. Significant differences were found between levels III and IV (P = .001), and levels III and V (P = .001), but not levels IV and V (P = .11).
Our results indicate that parents are accurate in reporting the daily mobility and function of their infants with moderate to severe motor delays using the PEDI-mob. Parent-reported PEDI-mob scores had a significant relationship with a therapist-administered GMFM-88 for infants younger than 2 years who had been diagnosed with CP or at high risk for CP. Based on GMFCS, children in this study had moderate to severe motor impairment, and PEDI-mob scores were found to vary as a function of GMFCS level. Including parents and caregivers in the evaluation of infants with CP and significant motor impairment may be an opportunity to improve functional outcomes following rehabilitation intervention.
Infants are being diagnosed with CP earlier, so it is important for physical therapists to have accurate tools to evaluate motor skills for a younger age group.6 The GMFM is known to be a valid, reliable, and responsive tool for evaluating motor capacity for children with CP.19,28 Previous work shows a significant relationship between the 66-item GMFM and the original version of the PEDI for older children with severe motor impairments.18 A positive correlation also exists between the PEDI-mob and the GMFM-88 for children older than 2 years across all ability levels on the GMFCS.13 Our results indicate that this relationship is also present in the first 2 years of life. This is important because, for younger infants and those with more severe motor impairment, there is less variability in motor skills, both at an individual level and at a group level. For example, all infants are working on skills such as head and truck control. Our results suggest that there is a strong relationship between a PROM and the GMFM even when there is less variability and more severe motor impairments.
There may be some challenges related to infant behavior when using the GMFM to assess the motor capacity of children younger than 2 years.29 For example, once a more advanced motor skill is mastered, such as creeping in quadruped, an infant may not perform more immature skills, such as belly crawling. If an infant refuses to display a more basic motor skill, the GMFM scoring accounts for this but may not fully represent the entire motor repertoire of that child. This is more of a concern for children who have already achieved crawling in quadruped compared with those who have not yet developed this skill.29 Moreover, if the abbreviated GMFM-66 version is used to assess an infant with more significant motor challenges, more basic skills, including belly crawling, are not included.19 Modifications to the GMFM-88 have been suggested when used to assess infants younger than 2 years who are crawling in quadruped.29 The infants in the present study were all GMFCS levels III, IV, or V. The descriptors for children younger than 2 years on the expanded and revised version of the GMFCS indicate that all children in this study would not yet be crawling in quadruped.30 This indicates to us that the GMFM-88 version is the best option for use to measure motor performance for our study population.
The infants included in this study had either an early CP diagnosis, a diagnosis of high risk for CP, or moderately to severely delayed motor development based on GMFCS level. Previous reports of GMFCS level distribution in children with CP indicate that the proportions in our study are atypical. In studies that include children across all GMFCS levels, levels III, IV, and V have similar proportions, ranging from 11% to 19% (level III), 11% to 26% (level IV), and 16% to 21% (level V).31–33 Our sample had fewer infants classified as level V (13%) than levels III and IV (31.5% and 37%, respectively). Children initially classified as GMFCS level V are not likely to be later reclassified, but it is more likely that children classified as levels III or IV would be later reclassified.34 It is known that GMFCS levels are more stable as children age.35 Our sample included infants younger than 2 years, and GMFCS levels are least stable in this age range. This may mean that infants included in our study are reclassified at a later time, and it is recommended that GMFCS level is reassessed over time.35 However, because the purpose of this study was to compare measures of motor function at a single time point, the potential for later reclassification is not likely to have impacted our results or interpretation.
Infants can be challenging to evaluate using standardized assessments, such as the GMFM, especially if they have a high level of medical fragility and complexity. Infants with higher levels of medical complexity and disability often fatigue quickly, so a parent-reported assessment could ease the burden of completing a lengthy physical assessment with these infants. Previous work indicates that parents can accurately assess the motor, cognitive, and communication abilities of their child with CP.36–38 PROMs might be preferred over extensive assessments for young infants with limited abilities to participate. The PEDI-mob can also be used remotely via telehealth if in-person or clinic-based services are difficult for families to access. This is a clear benefit when circumstances demand the use of telehealth for public safety, but the PEDI-mob can also be completed in settings where space, time, and equipment may limit a physical therapist's ability to administer the GMFM-88.39
Using PROMs, such as the PEDI-CAT, may support a collaborative parent-therapist relationship by acknowledging the value of information that parents have about their child.14 The PEDI-mob is efficient to administer. For infants, especially those who may have more complex medical needs, completing a full GMFM may not be possible. The PEDI-mob may offer a practical solution to obtaining accurate information about a child's motor skills. Lastly, while the GMFM provides valuable information about a child's capacity, the child's typical performance is captured by the PEDI-mob. Having information about a child's capacity and typical performance can inform care planning and goals for intervention. Interventions that address barriers to activity performance in daily life may promote participation.
This study had some limitations. There was a smaller sample of infants in GMFCS level V than in GMFCS levels III and IV. This may have contributed to the larger variance in PEDI-mob scores for this group. A sampling bias is also possible and would threaten the generalizability of these results. In consideration of this point, the racial demographics of our sample were explored and reported. The race of infants included is likely representative of local demographics, reducing this concern. This study tested only the relationship between assessment tools and did not take into account the child's participation in rehabilitation programs.
What This Adds to the Evidence
Our results indicate that the PEDI-mob accurately assesses the motor skills of infants with CP or at high risk for CP who have moderate to severe motor impairments. The PEDI-mob is a PROM that supports parent-therapist collaboration in motor evaluation. Having information from both a parent and physical therapist perspective can inform care planning and goals for interventions that enhance participation in daily tasks. The PEDI-mob can also be a practical solution for use if an infant is more medically fragile and longer or physically demanding assessments cannot be completed. Physical therapy practice has changed significantly with a recent increase in the use of telehealth visits. The PEDI-mob may be a tool for physical therapists to use when completing a telehealth evaluation.
We would like to acknowledge the persons in the Pediatric and Rehabilitation (PEARL) Lab for all of their work in the data collection. We would also like to thank the children and their families who participated in the DRIVE study.
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