Published online October 1, 2007
PEDIATRICS Vol. 120 No. 4 October 2007, pp. e880-e886 (doi:10.1542/peds.2006-2258)
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ARTICLE

Validation of the Gross Motor Function Measure for Use in Children and Adolescents With Traumatic Brain Injuries

Michaela Linder-Lucht, MD, Verena Othmer, MD, Michael Walther, MD, Julia Vry, MD, Ulla Michaelis, PT, Sabine Stein, PT, Heike Weissenmayer, PT, Rudolf Korinthenberg, MD, Volker Mall, MD and the Gross Motor Function Measure-Traumatic Brain Injury Study Group

Division of Neuropediatrics and Muscular Disorders, Department of Pediatrics and Adolescent Medicine, University Hospital Freiburg, Freiburg, Germany


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVES. Motor function recovery is a key goal during rehabilitation of children and adolescents with traumatic brain injury. To evaluate how well treatment strategies improve motor function, we need validated outcome measures that are responsive to change in pediatric patients with traumatic brain injury. The Gross Motor Function Measure has demonstrated excellent psychometric properties in children with cerebral palsy and Down syndrome, yet its responsiveness in patients with pediatric traumatic brain injury has not been proven irrefutably. Our aim was to validate the Gross Motor Function Measure for this patient group.

METHODS. Seventy-three patients (mean age: 11.4 years; range: 0.8–18.9 years) with moderate-to-severe traumatic brain injury were recruited in 12 rehabilitation centers and assessed twice with the Gross Motor Function Measure-88 over 4 to 6 weeks. As an external standard, we used judgements of change made independently by parents, physiotherapists, and 2 video assessors who were not familiar with the patients. We formulated and statistically investigated a priori hypotheses of how Gross Motor Function Measure change scores would correlate with those judgements of change. Both Gross Motor Function Measure versions, the original Gross Motor Function Measure-88 and the more recently developed Gross Motor Function Measure-66, were evaluated.

RESULTS. Both Gross Motor Function Measure change scores correlated significantly with all of the clinical judgements of change. The degree of correlation that we postulated, that the Gross Motor Function Measure change score would correlate highest with the video rating followed by physiotherapists and parents, was fully confirmed by the Gross Motor Function Measure-88 and largely confirmed by the Gross Motor Function Measure-66. Both Gross Motor Function Measure versions revealed convincing discriminative capability. Test-retest reliability was excellent.

CONCLUSIONS. We demonstrate convincing evidence of responsiveness and validity to support the use of both Gross Motor Function Measure versions as evaluative measures of gross motor function in children and adolescents with traumatic brain injury.

Key Words: GMFM-88 • GMFM-66 • GMFM • traumatic brain injury • children • adolescents • evaluation • motor function • validity • rehabilitation

Abbreviations: TBI—traumatic brain injury • GCS—Glasgow Coma Scale • GMFM—Gross Motor Function Measure • CP—cerebral palsy • T1—baseline measure • T2—measure after 4 to 6 weeks (±2 days) • T1R—measure readministered after 2 to 3 days • VA—video assessor

Traumatic brain injury (TBI) is a key cause of spastic movement disorders during childhood and adolescence. The estimated annual incidence of pediatric TBI in developed countries varies according to inclusion criteria, age, gender, and home country, ranging between 12 and 489 per 100000 (overall rate: 235 per 100000), with 2 peak periods of incidence in early childhood (age: ≤5 years) and between adolescence and young adulthood (age: 15–20 years). On the basis of initial scores in the Glasgow Coma Scale (GCS)1, 70% to 80% of patients are classified with mild TBI (GCS: 13–15). Moderate (GCS: 9–12) and severe (GCS: 3–8) TBI are reported in similar proportions of ~10%.2–6 Approximately 65% of children with severe TBI exhibit spasticity resulting in functional limitations and disability.7–10 Hence, recovery of motor function and achieving mobility are among the primary therapy goals during the rehabilitation of children with brain injury. The degree of motor function recovery is an important indicator of the rehabilitation methods’ efficacy. Although various rehabilitation programs have been designed to improve gross motor function in a pediatric population with TBI, there is limited research evidence supporting the effectiveness of these interventions.11 This might be because of the current lack of standardized evaluative measures with appropriate psychometric properties developed specifically for pediatric patients with TBI to assess the magnitude of functional change over time. Outcome assessments for this patient group are often self-developed, modified from existing measures, or incorporating a combination of cognitive, self-care, and physical dimensions without differentiation between mobility and purely motor skills, factors that complicate the interpretation of the amount of motor function recovery alone.12 The Gross Motor Function Measure (GMFM) is recognized in clinical practice and international rehabilitation research as the gold standard for evaluating quantitative changes in gross motor function. There are 2 versions of the GMFM available, the GMFM-8813 and GMFM-66.14 The GMFM-88 is the original criterion-referenced measure consisting of 88 items grouped in 5 dimensions of motor function: (1) lying and rolling; (2) sitting; (3) crawling and kneeling; (4) standing; and (5) walking, running, and jumping. It was primarily designed to detect clinically significant change in gross motor function in children with cerebral palsy (CP),13 followed by a comprehensive validation study for children with Down syndrome15,16 and a recent first-validation trial for children aged 5 to 17 years with spinal muscular atrophy.17 The responsiveness of the GMFM-88 to changes in motor function after TBI has also been partially established,13,18,19 but no comprehensive validation study for its application in this patient group has yet been conducted. The more recently developed GMFM-66 emanated from the GMFM-88 after applying the Rasch model of item analysis20 to it in an effort to improve its clinical usefulness. It is composed of a subset of 66 items, forming a 1-dimensional hierarchical scale. The GMFM-66 has only proved valid for children with CP so far, because the item difficulties were calibrated for use with that particular patient group. Aim of this multicenter study was to evaluate the validity of the GMFM-66 and GMFM-88 for use as responsive measures of change in motor function in children and adolescents with moderate and severe TBI during an inpatient rehabilitation setting.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Twelve rehabilitation centers in Germany (n = 11) and Switzerland (n = 1) participated in this study (study coordination center: Children's University Hospital Freiburg, Movement Disorders Study Group), recruiting children and adolescents between the ages of 1 and 18 years who received inpatient rehabilitation services for TBI. To ensure the necessary variability in population required for a validation study, we included patients in early and late rehabilitation phases; the interval between the time of injury and assessment was irrelevant. A detailed description of inclusion and exclusion criteria is provided in Table 1. It was not the aim of this study to evaluate therapy or early intervention services; thus, the patients were told to continue with their therapies at that time. The study was approved by the ethics committee of Freiburg University.


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  		TABLE 1 Inclusion and Exclusion Criteria

 
Determination of Validity
To establish a measure's validity, one must compare the measure of interest with the gold standard (criterion measure) for the factor being investigated (ie, motor function). There is currently no generally accepted gold standard in pediatric TBI rehabilitation centers for assessing quantitative changes in motor performance. Thus, rehabilitation researchers commonly use a construct as an external standard to validate the parameter in question. In accordance with the Canadian GMFM developers’ original validation study,13 we used the standardized appraisals of change made by parents, physiotherapists, and independent video assessors as an external standard, assuming that this measure reflects clinically relevant change in motor function. A priori hypotheses were formulated concerning how change scores on the GMFM would relate to change as judged by parents, physiotherapists, and independent video assessors.

First we postulated that changes in the GMFM scores would demonstrate a positive and significant correlation between the changes in motor function as rated by parents, physiotherapists, and independent video assessors (minimal correlation coefficient: >0.4) and that this degree of correlation would be higher between the GMFM change score and video rating (estimated correlation coefficient: >0.6) than between the GMFM change score and judgements of change made by parents and physiotherapists. We expected the lowest correlation to occur between GMFM change scores and those of parental appraisals. Our postulates were based on the consideration that standardized videotapes of motor function (rated by an independent assessor) would be considered the most objective, because the patient's actual performance would be recorded and evaluated (what is done versus what can be done). That value should correlate most closely with the GMFM measuring quantitative motor function. Because of their background knowledge about patients, motor function evaluations by treating physiotherapists are potentially biased. Parents, on the other hand, might perceive changes in motor function as reflecting improvement in everyday activities, a parameter usually differing considerably from the quantitative changes in gross motor function detected by the GMFM.

Second, we postulated that there would be fewer changes in gross motor function during the period between the actual injury and the first GMFM assessment. One would anticipate higher GMFM change scores reflecting faster change in motor function in the earlier rehabilitation phases.

Third, we also aimed to test and retest reliability of the GMFM in children and adolescents with TBI, considering the GMFM as reliable, provided the intraclass correlation coefficient for the total score attained ≥.90.

Evaluation
The assessment battery consisted of the GMFM, a standardized video recording, and standardized video rater, parent, and physiotherapist questionnaires. Evaluations were obligatory at baseline (T1) and after 4 to 6 weeks (±2 days; T2). The rehabilitation centers had the option of participating in an evaluation, including the GMFM readministered after 2 to 3 days (T1R), to monitor test-retest reliability.

GMFM
All of the physiotherapists who acted as GMFM assessors were trained in the use of the GMFM by the coordination center as a precondition for study participation. The official German translation of the GMFM-88 was applied, which had been developed by the Freiburg University Movement Disorders Study Group in 1999 in close cooperation with the GMFM's Canadian authors; it was recently published as the German GMFM manual.21 Training consisted of a 2-day workshop for beginners with no previous knowledge of the GMFM and a 1-day refresher course for certified users already familiar with the instrument. To monitor the reliability of the GMFM, all of the assessors were tested using a criterion test videotape to ensure that their scores achieved a minimum level of agreement (Somer's D coefficient: ≥0.7). The same physiotherapist assessed the GMFM at T1, T2, and T1R.

To investigate the GMFM-66 validity and sensitivity, all of the GMFM-88 raw scores were converted into the corresponding GMFM-66 scores using the computer software for the GMFM-66, the Gross Motor Ability Estimator.21 Validation analysis was repeated with the GMFM-66 values.

Video Assessments
The gross motor abilities of the study sample were videotaped during T1 and T2 according to a standardized protocol for camera position. Videotapes were <20 minutes long and contained samples of motor tasks of the lying and rolling; crawling and kneeling; sitting; standing; and walking, running, and jumping dimensions. Before the start of the study, physiotherapists were instructed in how to properly record the videotapes. The 2 video assessors were asked to rate the gross motor abilities observed and to judge any changes in overall and specific gross motor function dimensions using a standardized questionnaire. Motor abilities were rated using a 5-point Likert scale varying from 1 (no impairment) to 5 (very severe impairment). A 7-point Likert scale was applied to quantify the magnitude of change at the T2 assessment, ranging from –3 (much less) to +3 (much more), with 0 representing no change. They were explicitly instructed not to score the GMFM from videotape. Both assessors were blinded to the complete case histories of the patients, meaning they had no background information regarding rehabilitation phase, interval between brain injury and GMFM assessment, severity of TBI, motor and mental impairment, therapy goals, or other personal data.

Parent and Physiotherapist Questionnaires
The parent and physiotherapist questionnaires were identical to those of the video raters regarding the rating of current motor abilities and the magnitude of change at T2. In addition, information about the relevance of the observed change on everyday activities was obtained by parents and physiotherapists using a 7-point Likert scale ranging from –3 (severe negative impact) to +3 (highly positive impact). The questionnaires were administered by telephone by medical staff at the coordination center (2 pediatricians and 1 physiotherapist) according to a standardized protocol. The telephone interview took 8 to 10 minutes.

Statistical Analysis
All of the statistical computations were performed with SPSS 13.0 software (SPSS Inc, Chicago, IL). The criterion for determining significance was a P value of <.05 for all of the statistical tests. A Spearman's correlation coefficient was used for correlation analysis (hypothesis 1); the Mann-Whitney U test for independent samples was used to determine any gradient of change over time and whether the change in gross motor function decreased as the interval between brain injury and first GMFM assessment increased (hypothesis 2). Test-retest reliability (hypothesis 3) was evaluated using the Bland-Altman plot. Correlation between functional change and activities of daily living was examined by the Kruskal-Wallis test for k independent samples.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patient Characteristics
Of the 78 patients recruited in 12 study centers in Germany (n = 11) and Switzerland (n = 1) between October 2003 and August 2005, 5 failed to complete the study and had to be excluded from the analysis. A detailed description of the subject population is summarized in Table 2. The mean interval between the GMFM assessments was 5 weeks and 5 days (SD: ±7 days).


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  		TABLE 2 Baseline Characteristics of 73 Children With Moderate-to-Severe TBI Entered Onto a Prospective Multicenter Study to Evaluate the Validity of the GMFM-66 and GMFM-88

 
Hypothesis 1
Change scores for the GMFM, parent and physiotherapist questionnaires, and video ratings were derived by comparing total scores from T1 with those obtained at T2. Both GMFM version change rates and changes as judged by parents, physiotherapists, and video assessors correlated significantly, indicating parallel alterations (P < .0001). Correlations between the total GMFM-88 change score and video rating were best, meeting the hypothesized criterion of >0.6 (video assessor 1 [VA1]: r = 0.737; VA2: r = 0.657), followed by those between physiotherapists (r = 0.555) and parents (r = 0.531). In accordance with those results, we observed the highest correlation between the GMFM-66 change score and VA1 (r = 0.679), followed by those between physiotherapists (r = 0.609) and parents (r = 0.563). However, VA2 correlated much weaker than expected, with the GMFM-66 change score (r = 0.536) not achieving the hypothesized criterion of >0.6. We also assessed the reliability of the judgements of change made by the 2 independent video raters who were experienced physiotherapists. Interrater reliability was high, with r at 0.704 for the 9 overall judgements of change, ranging from 0.24 (sitting) to 0.726 (walking, running, and jumping) for the individual dimensions.

Hypothesis 2
As hypothesized, changes in gross motor function became fewer as the interval between brain injury and T1 increased. The total GMFM-88/-66 change scores in children and adolescents with date of injury >1 year before the first GMFM assessment (n = 10) was only 1.8% (SD: ±4.8%)/2.1% (SD: ±3.0), whereas it was 12.8% (SD: ±14.5)/11.6% (SD: ±10.3) in patients for whom the interval between brain damage and T1 was <1 year (n = 63). That correlation was statistically significant (P = .002/P = .001).

Hypothesis 3
Test-retest reliability of the GMFM-88/-66 was determined in a subsample of 10 children. The interval between T1 and T1R was 3.8 days (SD: ±1.1). The intraclass correlation coefficient for the total GMFM-88 and GMFM-66 score amounted to .99 (Fig 1).


Figure 1
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  		FIGURE 1 Bland-Altman plot for describing test-retest reliability with reference line to x-axis for doubled uncorrected SDs of GMFM-88 (upper continuous line) and GMFM-66 (upper interrupted line).

 
Correlation Between Functional Change and Activities of Daily Living
To investigate whether the functional changes observed in both GMFM versions were at all relevant to the patient vis-à-vis activities of daily living, we also compared parents’ and physiotherapists’ subjective judgments of the relevance of change with the GMFM's change score. Parallel alterations between GMFM change scores and parent and physiotherapist judgements regarding the impact of motor change on activities of daily living could be demonstrated (Table 3).


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  		TABLE 3 Correlations Between GMFM Change Scores and Parent/Physiotherapist Judgements Regarding the Impact of the Observed Change on Activities of Daily Living (n = 70)

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
We evaluated the validity of the GMFM-66 and GMFM-88 for use as responsive measures of change in motor function in children and adolescents with TBI in this study, using 3 a priori hypotheses, as described below.

First, change scores of the GMFM-66 and the GMFM-88 strongly correlated with all of the clinical judgments of change. For the degree of correlation, we postulated that the GMFM change score would correlate highest with the 2 video raters (VA1 and VA2) followed by physiotherapists and parents. This was fully confirmed with the GMFM-88 (r VA1 and r VA2 > r physiotherapists > r parents) and largely confirmed with the GMFM-66 (r VA1 > r physiotherapists > r parents > r VA2).

Second, change scores of the GMFM-66 and the GMFM-88 were higher during the first year of rehabilitation after brain injury than during later rehabilitation phases, reflecting the clinical observation that patients with TBI show the largest motor recovery during the first year of rehabilitation.22–24

Third, test-retest reliability in a small subsample of patients was high, indicating that both versions of the GMFM are consistent over a short period of time when no significant change in function occurred.

Using a priori construct hypotheses in the absence of a gold standard is a well-accepted validation strategy.13,15,25 The definition of a video rater as an objective observer is a crucial point in this validation method. In accordance with previous GMFM validation studies,13,15 the video assessors were physiotherapists blinded to the medical history of the patient, covering treatment, as well as statements from parents or therapists and/or medical professionals. They were not informed about the interval between the time point of brain injury and first GMFM evaluation. Because the video rater had to evaluate the question of change in motor function over time, and it was not our aim to investigate the impact of therapy or early intervention services, we did not blind the video raters to the time point (T1 or T2) of the assessments. Certainly, one could argue that an observer blinded for the time point of evaluation might be even more objective. However, we believe that we have eliminated the most serious confounders, and our video raters fulfilled the criterion of being highly objective and independent assessors.

This study did not evaluate interrater reliability in the administration of the GMFM. Taking into account that interrater reliability in children with CP and in those with Down syndrome has been excellent for trained users in the GMFM, it seemed reasonable to assume that the interrater reliability of trained users assessing pediatric TBI patients would be comparatively high.

Although our results indicate that both versions of the GMFM are valid and sensitive tools to assess change in motor function in pediatric patients with TBI, some differences are revealed between the 2 versions of the GMFM, however. In the GMFM-66, 1 objectivity criterion failed regarding the correlation between the GMFM-66 change score and VA2, indicating that the GMFM-66 might be less accurate in detecting clinically significant change than the GMFM-88. This finding might be explained by the development of the GMFM-66 representing a kind of concentration on the specific motor development pattern of patients with CP, which certainly differs from children with TBI. Because these differences between the 2 versions of the GMFM are nonetheless small and tend to be of merely theoretical interest, the potential advantages of the GMFM-66, namely its quicker administration and improved calculation of total scores (even when some items have been omitted), may enhance its clinical efficacy.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
This multicenter trial has provided sufficient evidence of responsiveness and the validity to support the use of the GMFM-88 and GMFM-66 in clinical and research settings as an evaluative measure of gross motor function in children and adolescents with TBI. A standardized therapy evaluation method is a precondition for a better understanding of therapeutic effects on motor outcome and for optimizing rehabilitative strategies in pediatric patients with TBI.


   ACKNOWLEDGMENTS
 
This study was financially supported by ZNS-Hannelore-Kohl-Stiftung grant 200 300 1.

The Gross Motor Function Measure-Traumatic Brain Injury Study Group participating in this trial included rehabilitation centers in Germany and Switzerland: University Children's Hospital Zürich, Rehabilitation Center, Affoltern (CH): B. Knecht, MD; Fachklinik Hohenstücken, Brandenburg: M. Köhler, MD; Neurologisches Rehabilitationszentrum Friedehorst, Bremen: M. Spranger, MD; HUMAINE Klinik, Geesthacht: A. Nolte, MD; Hegau-Jugendwerk Gailingen GmbH: D. Schmalohr, MD; Klinik Holthausen, Hattingen: W. Boksch, MD; Kinderkrankenhaus Park Schönfeld, Kassel: F.K. Tegtmeyer, MD; Klinik Bavaria, Kreischa: W. Deppe, MD; St Mauricius Therapieklinik, Meerbusch: K. Müller, MD; Fachkrankenhaus Neckargemünd: W. Diener, MD; Kinderklinik Schömberg: Ch. Seilacher, MD; and Behandlungszentrum Vogtareuth: S. Lütjen, MD.

We thank the children, adolescents, and their parents for participation. We especially thank the physiotherapists and pediatricians at all of the 12 participating rehabilitation centers for their invaluable assistance with data collection. We also thank Carole Cürten for editorial assistance.


   FOOTNOTES
 
Accepted Feb 19, 2007.

Address correspondence to Michaela Linder-Lucht, MD, Division of Neuropediatrics and Muscular Disorders, Department of Pediatrics and Adolescent Medicine, University Hospital Freiburg, Mathildenstrasse 1, D-79106 Freiburg, Germany. E-mail: michaela.linder{at}uniklinik-freiburg.de

The authors have indicated they have no financial relationships relevant to this article to disclose.


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 DISCUSSION
 CONCLUSIONS
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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics




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