European Journal of Paediatric Neurology 1999; 3: 714

ORIGINAL ARTICLE

Motor and perceptualmotor competence in children with Down syndrome: variation in performance with age
,1,2 EUGENIO MERCURI,3 TERESA RANDO ,1 TIZIANA PANTO ,2 MARIA SPANO 2 4 1 ANTONELLA GAGLIANO, SHEILA HENDERSON, FRANCO GUZZETTA
Department of Child Neurology, Catholic University, Rome; 2Department of Child Neurology, University of Messina, Messina, Italy; 3Department of Paediatrics, Hammersmith Hospital, London; 4Institute of Education, University of London, London, UK
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The aim of this study was to determine whether perceptualmotor competence in school-age children with Down syndrome was generally delayed or varied as a function of type of action. Twenty-two children with Down syndrome (13 males, 9 females), aged between 4.5 and 14 years were assessed on two standardized tests, the Movement Assessment Battery for Children (Movement ABC), a test of motor competence assessing gross and fine motor coordination, and on the Developmental Test of VisualMotor Integration, a test focusing on shape copying. In order to obtain a profile of each child's performance on the different items contained in the Movement ABC, the test was used in its extended form. This involves testing any child who failed an item appropriate for his/her level, at progressively lower levels until a base-line measure was obtained. All the children obtained scores below the 5th percentile for their age on both tests. However, superimposed on this delay, we found distinct variation as a function of task. Whereas some aspects of gross motor function showed age development with delayed but regular acquisitions, all the aspects of fine motor skills assessed were more severely impaired and showed little development with age. Accuracy and timing of tasks requiring bimanual coordination were most impaired in our sample while balance and ball skills showed more variability. These results suggest that intervention in the motor domain should be varied according to each child's particular profile of performance.
Keywords: Down syndrome. Movement ABC test. Developmental Test of VisualMotor Integration.

Introduction
Down syndrome (DS) is a condition which has provoked much scientific enquiry since it was first described over a century ago as a distinct clinical entity.1 In the area of perceptualmotor competence, there is no doubt that children affected by DS are less competent than their normal peers. Slightly more controversial is the idea that they may even be less competent on some motor tasks than other retarded children of similar intellect (see Refs 2, 3, for reviews).

A number of studies have shown that DS children follow a rather different pattern of motor development from normal children in the early years. In addition to the fact that the major milestones, such as sitting, standing, reaching and grasping are generally delayed, superimposed on this delay are some plateaux in development which are far more prolonged and tend to occur at different times than in their normal peers.3,4 At school age all these children have difficulty acquiring the movement skills expected of them and are often generally described as `clumsy'.5 They are slow to learn to use eating utensils and

Received 15.7.98. Revised 2.10.98. Accepted 3.11.98. Correspondence: Dr Eugenio Mercuri, Department of Paediatrics, Hammersmith Hospital, Du Cane Road, London W12 0HN, UK

10903798/99/03/0007+07 $18.00

& 1999 European Paediatric Neurology Society

8 writing implements, they find it hard to join in with other children in the playground because activities such as running or jumping are difficult. In younger children with DS, tests such as the Griffiths or Bayley scales have been used to document motor development.3,4,6,7 Although studies of school age children with DS do exist, the majority are experimental in nature and focus on underlying deficits which might account for the observed functional difficulties.4,5,8,9 Purely descriptive studies which attempt to look at strengths and weaknesses across a range of tasks are relatively rare. In the present study, we use a wide range of perceptuomotor tasks to describe the profiles of performance exhibited by children of school age with DS. The tasks presented to the children included gross motor activities, such as jumping and hopping, fine motor activities such as threading beads and cutting with scissors, as well as tasks requiring a combination of both gross and fine control, such as catching a ball. Our aim in examining the profiles of performance exhibited by the children is to determine whether the unevenness in the perceptuomotor development reported to be characteristic of children with DS in the early years is still present at school age or whether the variable rates of development have evened out to be replaced by a more generalized delay.

et al. Original article: M Spano our centre was also recorded. Cognitive ability was assessed by the centre's educational psychologist using the appropriate versions of the Wechsler scales (WPPSI for children under six and WISC for the others). Details of verbal, performance and global intelligence quotient (IQ) were made available to us.

Clinical examinations
All children in the study underwent a detailed neurological examination and were assessed on two points, which provide contrasting but complementary information on perceptualmotor abilities. The first, the Movement Assessment Battery for Children (Movement ABC)10 is a global test of motor competence, assessing both gross and fine motor coordination. The second, the Developmental Test of VisualMotor Integration11 is a much more narrowly focused test, requiring the child to copy a series of shapes of increasing difficulty.

Movement Assessment Battery for Children

The standardized test in the Movement ABC is designed for use with children aged 4 to 12+ years. A total of 32 items are divided into four sets of eight, each intended for use with children of specific ages. The first set of items, labelled age band 1 is designed for use with 4- to 6-year-old children, the second set, age band 2 for 7- and 8year-old children, the third for 9- and 10-year-olds and the fourth for children 11 years old and above. Within each age band, the structure of the test is identical. All children complete three items designed to assess mental dexterity, two items designed to assess the ability to propel or intercept a moving object, and three items which assess static and dynamic balance (see Table 1 for examples of tasks within each category). The Movement ABC test can be administered in a number of ways. When all that is required is a

Subjects and methods

Twenty-two children with DS, aged between 4.5 and 14 years, were included in the study. Thirteen were boys and nine were girls. All attended the Rehabilitation Centre of the Department of Child Neurology in Messina, Italy. Background clinical information was obtained from the parents or, when available, from the neonatal or paediatric files. Information about rehabilitative therapy preceding the attendance to
Table 1 Domain Manual dexterity Movement ABC: description of items Description

Item (examples) . . . . . . Peg insertion Threading beads Drawing between two lines which form a simple shape Bouncing and catching a ball in one-hand Throwing a bean bag into a box Walking heel-to-toe along a line

1. Speed and accuracy of unimanual movements 2. Bimanual coordination 3. Accuracy (preferred hand) 1. Receiving a moving object 2. Aiming an object at a fixed target 3. Dynamic balance (control of slow movements)

Ball skills Static/dynamic balance

Original article: Motor and perceptualmotor competence in children with Down syndrome measure of how a child compares with his chronological age peers, he/she need only be tested on one age band i.e. that appropriate for his/her age. Raw scores on each of the eight items are converted to scaled scores ranging from 0 to 5, with higher scores indicating poorer performance. Item scores are then summed to produce total scores (ranging from 0 to 40). Finally, percentile tables are consulted to determine how an individual compares with his/her age peers. In this study, we report each child's total score on the test supplemented by performance data on each of the eight items individually. Although a simple norm-referenced statement about a child is adequate for some purposes, it is often necessary to go beyond this level of assessment. Since in the present study, our objective was to determine whether the perceptuomotor development of children with DS was even across all tasks or varied systematically in some way, a more detailed profile of the strengths and weaknesses of each child was required. To achieve this the Movement ABC test was used as recommended by the authors in the section on `clinical/educational' uses of the test (p.118 of the manual). This involved starting at the appropriate age band as usual then continuing testing at lower levels until (a) the child passed the item or (b) no further testing was possible because the child had failed all items in that category. Using a downwards stepping procedure, performance was then scored as follows: if a child obtained a score of 4 or 5 on an item at the appropriate age band (i.e. below the 5th percentile), he/she was tested on the same item at the next lowest age band. This procedure was repeated until a score of 3 or less was obtained or the child failed completely. (NB This procedure, of course, could be only applied to children older than 6 years as for children below that age no lower age bands were available.) In order to obtain a measure of the degree of failure in each category of item, the following scoring system was then applied. One point was given each time a child failed the item at his/her own age level then additional points were given for failure on the lower age bands. A child passing an item in his/her appropriate age band would therefore have a score of 0 while progressively higher scores indicate that the child had failed one or more of the lower age bands. Using this scoring system, we were able to obtain: a) a detailed profile of test performance for each child in the study. Expressed in terms of `age equivalent' scores, we might find, for example,

that a child of chronological age 12 had `passed' on all three manual dexterity items in the test at the 9-year level (i.e. was able to achieve a score of 3 or less on that particular item), managed to pass the balance tasks at the 7-year level but failed to achieve even the 4year level on the tasks involving throwing and catching moving objects. b) more information on the level of performance achieved by the group as a whole on the different kinds of items in the test. This measure was obtained by summing the scores obtained by all children on each category of item.

Developmental Test of VisualMotor Integration (VMI)

This is a paper-and-pencil task11 in which a child copies a series of geometric shapes of increasing difficulty. The standard score reflects the accuracy of the copies and can range from 0 to 19; the lower the score, the less competent the performance.

Results
Clinical assessment
Karyotype information was available for 14 of the 22 children: this showed trisomy 21 in 13 children and a translocation in the other. No information was available for the other 8 children. All 22 children were born at term from uncomplicated pregnancies and all had a history of global neurodevelopmental delay. When they were referred to our rehabilitation centre, the children varied in age from 2 to 9 years. The duration and type of therapy received before referral was very varied and often discontinuous. Only 6 of the 24 children received early (i.e. started before 2 years) and continuous therapy.

Cognitive abilities
Full scale IQ ranged from 41 to 54, the verbal IQ from 45 to 55 and the performance IQ from 45 to 61. Table 2 shows details of the results of the cognitive assessment.

Movement ABC
On the Movement ABC all children obtained total scores below the 5th percentile for their age.

10 Figures 1, 2, and 3 show individual details of the level of performance. Here we plot each child's age equivalent score on each item in the Movement ABC. Table 3 shows the results of the within-group variation. To determine whether there was any evidence of systematic variation as a function of the type of task being performed, the results on the

et al. Original article: M Spano individual items were scored with a global impairment score. The scores in the whole group ranged from 25 (ball skills 2) to 56 (manual dexterity 2).

Developmental Test of VisualMotor Integration

All the subjects obtained low scores for their chronological age with their performance ranging from an age equivalent of 2 years to a maximum of 4 years, 2 months. None of the children was able to

Table 2 Full scale, verbal and performance IQ: individual results Age 4.9 4.6 4.11 5.4 6.3 6.9 7.9 7.8 8.6 8.10 9.5 9.2 10.6 10.2 11.11 11.6 12.4 12.5 13.6 13.10 14.3 14.7 Age band 1 1 1 1 1 1 2 2 2 2 3 3 3 3 4 4 4 4 4 4 4 4 Full scale IQ 52 54 45 49 45 51 44 48 41 41 44 46 41 43 49 41 46 44 42 45 42 44 VIQ 54 55 51 54 52 64 46 47 46 46 47 50 46 49 51 45 47 49 46 50 45 50 PIQ 58 61 51 53 48 47 51 58 45 47 50 51 45 48 54 45 50 49 47 50 45 46

Table 3

Global impairments scores Global impairment score

Manual dexterity Manual dexterity Manual dexterity Ball skills Ball skills Balance 1 Balance 2 Balance 3

38 56 45 44 25 39 35 44

A global impairment score was developed to produce a detailed profile of the strengths and weaknesses of each item in the whole group. For each item one point was given each time the child failed the item at his/her own age level then additional points were given for each failure on the lower age bands. The maximum score possible depended on the number of lower age bands available, with a minimum of 1 for age band 1 and a maximum score of 4 for age band 4 (the child fails the items on all 4 age bands). The global impairment score was produced by adding the individual results of all the children on that particular item.

Fig. 1. Level of performance (expressed as age equivalent) on the three items assessing manual dexterity.

Original article: Motor and perceptualmotor competence in children with Down syndrome

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Fig. 2. Level of performance (expressed as age equivalent) on the two items assessing ball skills.

copy any of the three-dimensional figures showing intersections. Figure 4 shows individual details of the level of performance.

Discussion
Many studies have reported motor impairment in children with DS which extends across the entire range of functioning, including both fine and gross motor skills.29,12,13 In agreement with these studies, our results also indicate that children with DS perform poorly in most areas of motor functioning. Although there was some variability in the level of performance, none of our children had scores adequate for their chronological age on either the Movement ABC or the VMI. The aim of this study, however, was not simply to replicate other studies but to try to determine whether all aspects of motor development at school age progressed evenly or whether there was systematic variation as a
Fig. 3. Level of performance (expressed as age equivalent) on the three items assessing balance.

function of task and/or age. Since the study was cross-sectional, our results must be treated with caution. Nevertheless, using the Movement ABC, we have been able to show distinct variations in performance that seem to be related to both age and type of task. For example, on some tasks, not a single child achieved age appropriate levels of motor competence and the gap between motor performance and chronological age appeared to become progressively wider. In contrast, for other

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et al. Original article: M Spano out the demands of the task and planning an appropriate motor output. The results on the items assessing gross motor abilities, in contrast, showed a wider variability. The two items assessing ball skills showed different results illustrating clearly the difference in the functions tested. While the ability to direct an object in space, such as hitting a target, was relatively maintained, the ability to adjust the body in space to receive a moving object and to anticipate the event was very poor and showed little improvement with age. Both static and dynamic balance were also affected, though a wider variability could be observed in these items. Attempts to explain the pattern of perceptuomotor impairment in DS are many and varied.1523 In the general population of individuals with mental retardation, the relationship between level of cognitive impairment, as measured by IQ, and motor competence has been explored in numerous studies. Since reported correlations rarely exceed 0.5 (leaving 75% of the variance in motor performance to be accounted for), there is now very little interest in pursuing this relationship further. In an exclusively DS sample, a slightly higher correlation between mental age and motor performance has been reported3 but this finding has not been replicated. In our study, the range of IQs obtained by the DS children was rather narrow (4145) with many of the children performing a floor level. The lack of variance associated with this floor effect prevented us from exploring the relationship between IQ and performance on our two perceptuomotor tests. However, in the light of previous findings, we consider it much more fruitful to look for other kinds of explanation for the various perceptuomotor difficulties experienced by DS children. Some of the earlier studies of children with DS focused on the presence of physical features associated with the syndrome which might affect performance.3,16,17 Poor results in manual dexterity for example, were attributed to the short fingers, flabby hands and lax ligaments which are a feature of DS. Similarly, hypotonia and lax ligaments in the hips were thought to be responsible for abnormal balance and gross motor difficulties. More recently, experimental studies have identified specific deficits in aspects of visuomotor integration, eyehand coordination, and balance all of which point to impairment in much higher levels of motor control.3,12,13,21 Neuropathological studies,18 and more recently magnetic resonance imaging studies20,21 have clearly demonstrated that in individuals with DS both the cerebellum and the brainstem look smaller. The incomplete development of these

Fig. 4. Level of performance (expressed as age equivalent) on the Developmental Test of VisualMotor Integration.

aspects of motor functioning, delays were clearly present but the amount of discrepancy between level of performance and chronological age remained relatively stable, irrespective of the child's age at assessment. We were also able to demonstrate the taskdependent variation in performance in another way. By averaging scores across all subjects, it was clear that some skills were consistently worse than others irrespective of age. Unlike previous studies which have suggested that fine motor skills might be less affected than gross motor skills,13,14 our results have shown that all the aspects of fine motor skills we assessed were severely impaired in all the children examined, irrespective of their age. Of the three tests assessing manual dexterity, the one which focuses on accuracy and timing in bimanual coordination yielded the highest impairment score in the whole test with the degree of impairment much more evident in the older children. With one exception, no child over the age of 11 achieved the level expected of a normal 7year-old. Considerable impairment was also evident in both the manual dexterity task which assesses timing and accuracy in both hands tested separately and in that evaluating visuomotor integration by testing the accuracy in tracing a line between boundaries. A deficit in visuomotor skills was further demonstrated in our cohort by the VMI test which showed progressively low scores with age. In these children the lack of accuracy in drawing the line was only part of the problem as even the oldest children had major problems with the more complex three-dimensional figures showing intersections. As the figures to be copied increased in complexity, it was clear that the DS children had no strategies for working

Original article: Motor and perceptualmotor competence in children with Down syndrome structures might therefore play a role in the integration of the sensory input and in the dexterity and coordination of movement. In conclusion, our results suggest that the delayed perceptuomotor development exhibited by all children with DS is not evenly distributed across all tasks. Although we have used only a small number of the vast range of motor tasks we might have used, our results suggest that the degree of impairment in gross motor abilities seems to remain relatively similar irrespective of the age when the test was performed. In contrast, fine motor skills, especially bimanual skills and skills requiring fast responses to moving objects do not seem to progress at the same rate. This seems to be especially true when the perceptual demands of the task are high and there are tight time constraints. As we have already noted, the fact that this was a cross-section, rather than longitudinal study means that our findings must be interpreted with caution. Moreover, since few of the children in this study had received early and regular intervention programmes, we must consider the possibility that the pattern of results we have obtained might not be generalizable to all DS populations as we cannot exclude that children who receive early and regular intervention programmes might show better development, as previously shown.14,23,24 Nevertheless, our results clearly indicate that some areas of motor abilities, especially in absence of rehabilitation seem to be more affected than others, suggesting that these might be the target for early intervention.

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7 Ramsay M, Piper MC. A comparison of two developmental scales in evaluating infants with Down syndrome. Early Hum Dev 1980; 4: 8995. 8 Kerr R, Blais C. Motor skills acquisition by individuals with Down syndrome. Am J Ment Defic 1985; 90: 313318. 9 Berkson G. An analysis of reaction time in normal and mentally deficient young men, I, II, and III. J Ment Def Ref 1960; 4: 5157. 10 Henderson SE, Sudgen D. The Movement Assessment Battery for Children. London: Psychological Corporation, 1992. 11 Beery KE. The Developmental Test of VisualMotor Integration (Revised edition). Cleveland OH: Modern Curriculum Press, 1982. 12 Frith U, Frith CH. Specific motor disabilities in Down's syndrome. J Child Psychol Psychiat 1974; 15: 292301. 13 Connolly BH, Michael BT. Performance of retarded children with and without Down syndrome, on the Bruininsk Oseretsky Test of Motor Proficiency. Phys Ther 1986; 66: 344348. 14 Connolly BH, Morgan SB, Russell FF, Fullton WL. A longitudinal study of children with Down syndrome who experienced early intervention programming. Phys Ther 1993; 73: 170181. 15 Schapiro MB, Haxby JV, Grady CL. Nature of mental retardation and dementia in Down syndrome: study with PET, CT and neuropsychology. Neurobiol Aging 1992; 13: 723734. 16 LaVeck B, LaVeck GD. Sex differences in development among young children with Down syndrome. J Pediatr 1977; 91: 767769. 17 Reed RB, Pueschel SM, Schnell RR. Interrelationship of biological, environmental and competency variables in young children with Down syndrome. Appl Res Ment Retard 1980; 1: 161165. 18 Crome LC, Stern J. Pathology of Mental Retardation London: Churchill, 1976.

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