RELATION OF GAIT ANALYSIS TO GROSS MOTOR FUNCTION IN CEREBRAL PALSY

Diane L Datniatro Mark F Abel

Human walking is a complex process which involves the integration of neural signals leading to muscle contraction and subsequent joint motion. Computerized motion analysis laboratories have enhanced the clinical evaluation and sci- entific study of human walking in normal and pathological conditions (Sutherland et al. 1988, Perry 1992). Gait analysis has been used extensively in cerebral palsy (CP) to evaluate the complex gait abnor- malities in these patients, often involving more than one joint. and to assess the effects of intervention in this population (Sutherland 1978. Thometz et al. 1989, deLuca 199 1 , Gage 199 1 ).

Two assumptions implicit in the use of gait analysis for assessing ambulation in children with CP are ( I ) that walking is an important skill to these children and their families (Bleck 1990), and (2) that gait performance is representative of overall gross motor skill (Smidt 1990). Nearly 70% of all children with CP even- tually ambulate (Molnar 1979); howev’er, their patterns differ qualitatively from normal pediatric gait (Rosenbaum er d. 1990). Children with spastic CP typically have slower gait velocities, due primarily to restrictions in stride length rather than cadence (Abel and Damiano 1996). Kinematic parameters differ in that joint motions can be either restricted or exag- gerated, depending on the extent of neurological involvement and the com- pensatory mechanisms used (Winters et C J ~ . 1987, Thometz er uI. 1989). Joint moments and powers can also vary from normal at a given joint in both magnitude

and pattern. or in the distribution of forces across joints (Perry 1992). Children with CP have a greater energy cost associated with walking (Rose er al. 1989). and their ability to ambulate tends to deteriorate with age and growth (Norlin and Odenrick 1986).

Walking is not the only motor skill impaired in these children. Depending on. the distribution and severity of motor involvement, other fine and gross motor skills may also be compromised in an individual with CP. The Gross Motor Function Measure (GMFM) has been developed recently to document motor status and to measure change over time or as a result of an intervention in children with CP. This measure encompasses a range of motor activities that a child might employ throughout the course of a day, and includes five dimensions: ( I ) lying and rolling, (2) sitting. (3) crawling and kneeling, (4) standing, and (5) walk- ing, running and jumping.

The purpose of the GMFM is to quan- tify how much motor function the child is able to demonstrate. This measure has been validated for use in children with CP. and has excellent intra- and inter- tester reliability. The GMFM has been correlated with other measures such as isokinetic strength (Kramer and MacPhail 1994) and peak aerobic power (Parker et al. 1993). GMFM scores have been reported alongside gait parameters but no attempt has been made to deter- mine the relationship between these assessments in the evaluation of children with CP. Both the GMFM and gait

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analysis have been proposed as valid indicators of motor skills in CP and as instruments to evaluate change, but is the information provided by these measures complementary, redundant or conflict- ing?

This study examined whether walking ability is representative of overall gross motor performance and, if so, to what degree. Multiple parameters are quanti- fied in a gait assessment, yet no study has previously addressed the question of which are the most related to or predic- tive of gross motor function. It was hypothesized that time and distance para- meters would demonstrate the strongest relationship with motor scores since these a$ the end result of multiple factors such d-dynamic balance, joint excursion and fdrce production. A second goal was to a k s s the differences in gait measure- ments and GMFM scores based on the

Qevel of functional motor involvement in children with CP. This project was a pilot investigation to explore the individual and relative contributions of each of these measures to the assessment of 'children with CP at a single point in time. Our ulti- mate research goal is to use gait analysis and the GMFM in an outcomes study which examines the effects of soft-tissue surgery over time on motor function in CP.

Method SUBJECTS Thirty-two children with spastic CP par- ticipated in this project. The mean age of the children was 8.9 (range 3 to 18) years. Twenty six of the children were diag- nosed as having spastic diplegia, while six had spastic hemiplegia. Diagnostic categories within CP are based on the nature and distribution of the neuromus- cular impairment. All patients exhibited spasticity, which is a heightened velocity- dependent response to passive muscle stretch, due to pyramidal tract pathology. Patients with extrapyramidal signs (athetosis or ataxia) were excluded from the study group. Patients with significant mental retardation or medical conditions affecting endurance in our laboratory set- ting were also excluded. Children with the diplegia classification demonstrated motor dysfunction primarily in the lower

extremities, while those with hemiplegia showed an impairment in the upper and lower extremity on one side of the body. All participants had been referred to the motion analysis laboratory for a clinical gait evaluation. in consideration of the need for surgical or orthotic intervention, or for a baseline assessment of their ambulatory status. None of the children had undergone surgery in the previous year. Although the study group was a sample of convenience rather than of ran- dom selection, the participants did span the range of ambulatory abilities observed in the general population of children with CP who are able to walk.

Each child underwent three-dimen- sional gait analysis at a freely selected 'normal' speed which included capture and processing of time and distance, kinematic and kinetic data. After the clinical gait assessment had been com- pleted, the GMFM was administered in the laboratory by the same physical ther- apist who conducted the gait assessment. Functional ambulatory status was deter- mined through observation coupled with parent report, and the children were then subclassified into one of three groups. Group 1 consisted of 12 children who were independent ambulators at all times; group 2 consisted of five children who were able to ambulate independently but needed assistive devices for some com- munity excursions; and group 3 consisted of 15 children who required assistive devices for ambulation at all times. This classification was similar to . that described by Hoffer and co-authors (1973), except that the community ambu- lators (Hoffer level 1 ) were further subdi- vided in this study as two distinct groups (groups 1 and 2). Group 3 wa. equivalent to Hoffer level 2, and no patients in Hoffer levels 3 and 4 (non-ambulators) were included in this study. Since the purpose of this project was to assess the relation between evaluative measures in ambulators, this modification allowed greater delineation among ambulators than the Hoffer classification. Our earlier study had demonstrated that dependence on walking aids was directly related to walking speed and gait efficiency (Abel and Damiano 1996); therefore this is a valid means of further delineation of

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TABLE I Gait parameters and GMFM scores of 32 children with cerebral palsy

Parameters Mean (SD)

Time and distance Velocity (m) 0.74 (0.31)

Cadence (stepshin) 119 (31.8) Double support (% of gait cycle) 31.8 (10.9) Single support (% of gait cycle) 33.9 (6.65)

Stride length (m) 0.73 (0.21)

Excursion in sagittal plane (degrees) Pelvic tilt Hip Knce Ankle , .

Peak joint moments ( N m/kg)' Hip extensor Hip flexor Knee extensor Knee flexor Ankle plantarflexor Ankle dorsiflexor

GMFM scores(%) Dimension 1 Dimension 2 Dimension 3 Dimension 4 Dimension 5 TOTAL

8.81 (3.23) 45.4 (9.47) 41.4 (12.9) 32.0 (14.7)

83.5 (37.8) 80.9 (37.8) 57.1 (29.7) 43.0 (28.4) 101 (32.5) 18.5 (19.7)

97.3 (2.91) 95.3 (7.86) 90.4 (14.2) 65.5 (28.2) 52.5 (33.6) 81.2 (15.2)

'Data are for 26 of the 32 children

functional ambulatory groups. Twenty seven of the children routinely used ankle-foot orthoses when ambulating, although for the purposes of the present study all assessments were performed with the child barefoot.

GAIT ANALYSIS Children were instructed to walk barefoot down a 12m carpet strip in the center of the laboratory at their regular walking speed, with hand-held assistive devices if needed, until three trials were obtained. Each child was allowed to rest between trials if needed, so that fatigue was not a factor. A four-camera motion-analysis system was used to obtain data. Once the three-dimensional co-ordinates were obtained, the Vicon Clinical Manager computer program (version 1.2 I , Oxford Metrics Limited, Oxford, UK) was used to process all data. A mean value for each

of the following parameters was com- puted for each child: velocity, stride length, cadence, percentage of the gait cycle spent in single support, percentage spent in double support, total excursions in the sagittal-plane at the pelvis, hip, knee and ankle. and peak sagittal plane moments at the hip, knee and ankle. Kinetic data could not be obtained for six children because of inadequate step lengths or due to assistive devices con- tacting the force plates. For inter-subject comparisons, velocity and stride-length values were normalized by dividing the actual value by each child's leg length as measured segmentally from the greater trochanter to the floor. Electromyographic data were obtained on many of the subjects as part of their clini- cal evaluation, but since these data are pri- marily descriptive rather than quantitative they were not included in the analyses.

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TABLE 11 Mean of all parameters for 32 children' with cerebral palsy, according to ambulatory function

Parumeters Groiip I Group 2 Group 3 Differences' (N = 12) (N = 5 ) (N = 15)

7.25 12.1 9.07 I .53 1.18 0.83 1-3

Normalized stride length I .28 1.18 0.92 1-3 Cadence 141 I20 100 1-3 Double support percentage 26.0 27. I 38.0 1-3 Single support percentage 37.7 36.4 30. I 1-3

Hip 49.7 49.0 40.8 1-3

Age Normalized velocity

Excursion in sagittal plane

Knee 45.8 41.4 37.8 NS Ankle 28.6 23.8 37.4 NS

Hip extensor 76.4 82.2 93.2 NS Hip flexor 76.8 105 81.8 NS Knee extensor 45.7 80.6 59.7 NS Knee flexor 36.3 48. I 50.7 NS Ankle plantarflexor 98.1 126 89.5 NS Ankle dorsiflexor 21.0 10.2 20.2 NS

Dimension I 98.8 97.2 96.3 NS Dimension 2 99.2 97.6 91.5 NS Dimension 3 97.0 91.4 84.7 NS

Peak joint moments (N mkg)'

GMFM

Dimension 4 86.9 79.4 44.0 1-3, 2-3 Dimension 5 79.7 72.2 24.2 1-3. 2-3 Total 93.4 87.6 68.4 1-3. 2-3

'Data for moments were available for only 26 of the 32 children. 'Significant results of one-way 'ANOVA across groups ($1~0.05)

FUNCTIONAL ASSESSMENTS The GMFM was administered to each child in addition to the gait assessment. A single examiner. who was trained by the test developers and met established relia- bility criteria, performed all GMFM test- ing. The total score and the scores for each of the five dimensions were used in data analyses.

STATISTICAL ANALYSES To assess the relationships among gait parameters and GMFM scores, multiple regression was used. The correlation matrix obtained from this procedure was used to describe relationships between pairs of variables. The dependent variable used in this procedure was the GMFM total score. All gait parameters collected during the assessment were entered as independent variables to determine which parameter or combination of parameters best predicts GMFM performance.

The magnitude and direction of differ- ences among groups in gait parameters and GMFM scores were shown descrip-

392 tively through a listing of the mean

values for each variable across the three ambulatory levels as outlined above. To find out if the groups differed statisti- cally. multiple one-way ANOVA proce- dures were performed for each parameter across groups, followed by Scheffe post hoc analyses when warranted.

Results The means and standard deviations of all variables measured are shown in Table 1. All means are based on 32 subjects, except for the means for the joint moment data which include only the 26 children who contacted the force plates correctly during the walking trials. The 32 children were then subcategorized into three groups according to ambulatory function, and the values of the gait parameters and GMFM scores across groups are listed in Table 11, with significant inter-group dif- ferences on ANOVA (~~0.05) presented in the last column. With the exception of the kinetic data and ankle excursion, all parameters increased or decreased incre- mentally as functional involvement wors- ened. The mean values moved further

TABLE I11 Significant bivariate correlations relating gait parameters to GMFM scores for all 32 subjects

Coitiparisotts r

GMFM total score with: Normalizcd stride length Normalized velocity Cadence Sagittal plane hip excursion Sagittal plane knee excursion Double support% Single support %

0.600 0.720 0.793 0.362 0.553

-0.498 0.494

P

0.014 0.000 0.000 0.04 I 0.003 0.007 0.007

from established normal pediatric values as described in the literature (Sutherland et nl. 1988, Wheelwright et af. 1993) as functional level decreased, except for cadence, which was exaggerated in the most highly functional group (group 1). and moved closer to or slightly below the normal value in the less functional groups (2 and 3).

All time and distance parameters, and GMFM scores except for dimensions 1. 2 and 3, differed significantly bctween the highest and lowest functional groups. Considering the sagittal plane kinematic data, only hip excursion was found to dif- fer significantly between groups 1 and 3. The GMFM scores for dimensions 4, 5 and total score also differed significantly between group 3 and the next highest level of function (group 2). Interestingly, the 12 children who comprised group I also had the 12 highest GMFM scores. However, none of the parameters was found to differ significantly between the two higher groups (1 and 2), despite con- sistent incremental differences. No statis- tical differences were found in the joint moment data across groups.

In assessing the correlation between the GMFM and gait parameters, cadence, normalized velocity and normalized stride length were found to be positively related to the GMFM total score. Hip and knee excursion were also directly related to the GMFM score, whereas ankle excursion showed virtually no relation. The percentage of the total gait cycle spent in single support was positively related to the GMFM score, with the per- centage spent in double support being

inversely related (Table 111). The results of the stepwise multiple

regression procedure indicated that cadence alone was a significant predictor of GMFM total score, alone accounting for 60% of the variance in GMFM score (R=0.76). No other variables added sig- nificantly to the prediction.

Discussion The GMFM and gait analysis are com- monly used to assess patients with CP. but it is not certain how one test relates to the other in the overall evaluation of these children. The primary aim of this investigation was to assess the relation betwecn clinical gait analysis and the GMFM in children with CP. Based on this sample of 32 ambulatory children with spastic CP, gait status was shown to be clearly representative of overall motor function in this population. Findings that support this inter-relationship include: ( 1 ) the strong bivariate correlations between gait variables and GMFM total score, and (2) the fact that the 12 highest GMFM scores were seen in the 12 children with the highest functional ambulatory rating.

As hypothesized, time and distance parameters - in particular cadence and normalized velocity - showed the highest correlations with gross motor function. This is hardly surprising, since these measures encompass relatively more information than kinematic or kinetic parameters that focus on motion or force at a single joint. Significant but weaker correlations with motor score were found for stride length, hip and knee excursion, and single and double support times.

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Since the magnitude of each of these parameters also varies systematically with velocity, the unique relation of each to gross motor function is difficult, if not impossible, to decipher.

An unexpected finding was the emer- gence of walking cadence as a strong and significant predictor of GMFM score. The regression analysis showed that cadence was particularly important in predicting motor status in CP. Cadence decreased across groups, beginning above normal in group 1 (the most func- tional) and dropping to below normal in group 3 (the least functional). Restrictions in stride length due to static or dynamic contractures are characteristic of the gait in CP and alterations of walk- ing speed are achieved primarily by mod- ulating cadence (Abel and Damiano 1996). The present study suggests that the free walking speed is decreased in the more neurologically involved because neither adequate stride length nor the compensatory increase in cadence is achieved.

When the patients were grouped by functional ambulatory ability, differences were found in both quantitative gait para- meters and GMFM scores. With the exception of joint moment data and ankle excursion, a gradient was seen in gait and GMFM values. As the level of ambula- tory independence decreased, mean val- ues became progressively further from pediatric norms. This finding supports the validity of our functional classification based on the need for walking aids, and confirms the results of an earlier study on a different sample of children with spas- tic diplegia showing a decrease in veloc- ity, stride length, and hip and knee excursion, with an increase in double support time, as a function of increasing neurological involvement (Abel and Damiano 1996).

Similarly, motor scores obtained with the GMFM were found to differ signifi- cantly between functional groups in the standing and walking dimensions as well as the total score. As neurological involvement increases, broader aspects of motor execution are disturbed in CP. Delays in the acquisition of major motor milestones, such as sitting and standing, are related to extent of neurological

involvement and carry a poor prognosis for ambulation (Bleck 1975). This study confirms that the GMFM scores, which reflect the ability to perform complex movement patterns incorporating trunk balance and co-ordination, also differ as a function of neurological involvement. Furthermore, the results suggest that GMFM dimensions 4 and 5 may be the only ones that need to be administered in order to assess differences across ambu- latory groups.

When evaluating the effects of a thera- peutic intervention on gait, results from the present study predict that the direc- tion of change in gait parameters should be the same as i n GMFM scores. Therefore it is conceivable that either assessment could be used to evaluate the effects of treatment. However, we would suggest that to evaluate an intervention aimed at improving walking, gait analysis is the optimal choice because it allows one to focus on the specific joints tar- geted. by the intervention. Furthermore, as shown by this study, velocity, cadence and stride-length measurements obtained through gait analysis provide an insight into more global motor functions. A treat- ment such as muscle-lengthening surgery may improve gait while adversely affect- ing other motor skills due to a weakening effect. The GMFM could then broaden the functional assessment by evaluating other skills that challenge different mus- cles from those used when ambulating, or the same muscles to a different degree. It is important to reiterate that while gait analysis and the GMFM are highly corre- lated, they do not measure the same thing; therefore complete agreement across the two measures would not be expected, nor would it necessarily be desirable. Another differentiating factor is that gait analysis is restricted to ambu- Iators, whereas the GMFM can be used to evaluate all children with CP regardless of ambulatory status. In our laboratory, we are currently using the GMFM in con- junction with a detailed physical exami- nation to assess surgical outcomes for pre-ambulatory patients.

A major dilemma for clinicians and researchers who assess treatment of patients with CP has been the broad het- erogeneity of patients with this diagnosis.

Attempts have been made to classify ambu- latory patients on the basis of kinematic patterns (Winters er al. 1987) - although this study and our earlier one have indicated that time and distance measurements show the greatest differences among CP groups (Abel and Damiano 1996). Of the kine- matic and kinetic measurements consid- ered, only hip excursion showed significant inter group differences. GMFM scores also show similar predictable incremental changes in different functional subgroups of children with CP, and may even show greater discfiminative ability since this measure, in contrast to gait parameters, was able to statistically distinguish the two lower groups. We have begun to explore the use of gait analysis parameters and the GMFM scores to discriminate mathemati- cally among groups of ambulatory children with CP. It is likely that multiple parame- ters, including subsets of gait data and the GMFM, considered together may prove to be the best method of delineating different functional groups before assessing the effects of an intervention.

With respect to evaluating change in walking and other motor skills. both gait analysis and the GMFM have been shown to be responsive, but their relative sensi- tivities have not been explored. Theoretically, improvement in the GMFM would requirc acquisition of a new motor skill; whereas gait analysis

since it provides multiple measurements of a single skill (walking) may detect smaller changes. As a counterpoint, everyday life involves the execution of multiple motor tasks in addition to walk- ing. While gait analysis may be a more exact measurement of changes in walk- ing, the GMFM may prove more essential in detecting clinically significant changes that affect the quality of life. Thus the combined use of gait analysis and the GMFM may enhance the responsiveness of the evaluation process to subtle yet significant changes.

In conclusion, this study provides fur- ther evidence that clinical gait analysis and the GMFM are valid indicators of motor function in CP. However, the underlying mechanisms that differentiate levels of motor function in the heteroge- neous diagnostic category of CP, and the relative sensitivities of GMFM and gait analysis, remain to be determined. Accupredji)r prtblrcrrriuri 25ili Mu\ 1995.

Ar~rro~iledgrmerrr.~ We gratefully acknowlcdge support for this project from the Orthopacdic Research and Education Foundation (OREF # 94-106).

Airtliors * Appoiirrmerirs Diane L Damiano, PhD, IT; *Mark F Abel, MD: Department of Orthopacdics. University of Virginia. Kluge Children's Rchabili~ation Center, 2270 Ivy Road, Charlottesville. VA 22903. USA.

"Corrrspoiideiics 10 cecoird mrhor. 1

SUMMARY The Gross Motor Function Measure (GMFM) and computerized gait analysis are commonly used to assess patients with cerebral palsy (CP). The authors investigated correlations between the GMFM and gait parameters in 32 children aged 3 to 18 (mean 8.9) years with spastic CP. Of the gait paramcters. cadence and normalized velocity correlated most strongly with the GMFM score. and hip and knee excursion and percentage single support also correlated directly with the GMFM. In a stepwise multiple regression, cadence alone was a significant predictor of GMFM score. Time and distance parameters. hip and knee excursion in the sagittal plane and GMFM values all moved consistently further from pediatric norms as functional severity increased. The study confirms that gait is representative of general motor status in CP and that the GMFM and gait analysis are complementary measures in the functional assessment of these children.

Rrlatiotis etrtre I'ntrolyse de lrr d@ttrorche et le troirble iiioteirr glohrrl dam I'IMC Une evaluation du trouble moteur global (GMFM) et une analyse de la demarche par ordinateur a 616 pratiquee systematiquement pour caracttriser des IMC (CP). Les auteurs ont recherche les corrdations entre le GMFM et les parametres de la demarche chez 32 enfants iges de 3 h 18 ans (moyenne 8.9) presentant une IMC spastique. Parmi les parametres de la demarche. les correlations les plus elevdes avec le GMFM concernaient la cadence et la vitesse normaliske; I'excursion de la hanche et du genouet le pourcentage de support unipodal prksentaient Cgalement une correlation directe avec le GMFM. E m s une analyse de variance B regression multiple. la cadence h elle seule etait predictive du score GMFIM. Les parametres de distance et de temps. I'excursion de la hanche et du genou dans un plan sagittal et les valeurs GMFM s'eloignaient des normes pkdiatriques avec

RESUME

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la gravite fonctionnelle. Cctte etude confirme que la demarche cst un reflet de I’Ctat moteur global dans I’IMC et que le GMFM et I’analyse de la demarche sont des mesures complkmentaires dans I’evaluation fonctionnelle dcs enfants examinks.

ZUSAMMENFASSUN.G Beziehiiiig zwisclieri Gnrtgariulwe iiiid grobiriotorisclier Fuiiktiori bei Cerebrnlparese Der Gross Motor Function Measure (GMFM) und die Kornputerganganalyse .werden in der Regel zur Beurteilung von Patienten mit Cercbralparese (CP) herangezogen. Die Autorcn untersuchten die Zusammenhange zwischen dem GMFM und Gangparametern bei 32 Kindern mit spastischer CP’im Altcr 3 und 18 (itn Mittel 8.9) Jahren. Von den Gangparametern korrelierten Kadenz und geregelte Geschwindigkeit am starksten niit dem GMFM Score und auch der Huft- und Knieexcursion und der Anteil des single support korrelicrten direkt niit dem GMFM. Nach einer schrittweisen rnultiplen Regressionsanalyse blieb nur noch die Kadcnz als signifikanter Parameter fur den GMFM. Zeit und Entfernungsparametcr, Huft- und Knicexcursion in einer sagittalen Ebene und GMFM Wcrte entfernten sich mit zunehmendcr Funktionsverschlcchterung von dcn padiatrischcn Norrnalwerten. Die Studie bestiitigt, daR der Gang fur den allgemeinen motorischen Status bei Cerebralparesc repriisentativ ist und daR der GMFM und die Ganganalyse komplementare Methoden fur die funktionelle Beurteilung dieser Kinder sind.

RESUMEN Relncidri del ciritilisis de Iti rriorchn coil Iti fiiricio’ri rriotorn grosern eii lo pcirtilisis cerebral La Medici6n de la Funci6n Motora Grosera (MFMG) y el aniilisis cornputarizado de la marcha se usan corrientemente para cvaluar. los pacicntes con paralisis cerebral (PC). Los auiores investigaron las correlaciones cntre la MFMG y 10s parimetros de la marcha en 32 niiios de 3 a 18 aiios (promedio 8.9) con PC espistica. De 10s parirnetros de la marcha, la cadencia y la velocidad normalizadas sc correlacionaban muy fuertementc con el puntage de MFMG; el recorrido de la cadera y la rodilla y el porcentage de soporte simple apoyan tambifn la corrclacicin directa con el puntage MFMG. En una regresi6n mliltiple del paso. la cadencia sola era un predictor significativo del puntage MFMG. Los pariimetros de ticmpo y distancia, la excursicin de cadera y rodilla en un plano sagital y 10s valores de MFMG todos son factores aiiadidos a las normas pediatricas con mayor valor al aumcntar la gravedad funcional. El estudio.confirma que la marcha es representativa del estado motor general en la PC y que el anilisis MFMG y de la marcha constituyen medicioncs complementarias en la evaluaci6n funcional de estos niiios.

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