Advances in the fields of obstetrics and neonatology have improved the survival of children born preterm. However, this improvement is associated with considerable morbidity.1

Recent studies have shown that compared to their peers, many children born preterm considered to be free of neurological sequelae experience difficulties in some developmental areas that may go unnoticed until school age, such as coordination, balance, or attention.2,3

The acquisition of motor skills and control is a long process that starts with newborn reflexes and continues throughout the lifespan and is influenced by environmental factors and the performance of motor activities during development.4,5 Visual-motor integration is defined as the immediate and precise response that takes place following the appearance of an object in the visual field.6 Developing adequate coordination requires having an adequate body scheme combined with adequate afferent sensory information and control over the existing body scheme, which allow an effective motor response.

Postural control is defined as the ability to sustain balance by maintaining the body centre of gravity on the base of support.7 From a biomechanical perspective, we use the term “balance” to refer to the dynamics of body posture to prevent falls, which is related to the forces that act on the body.8 Maintaining balance requires the integration of the information provided by the proprioceptive, vestibular and visual systems.

There are different tools to assess motor competence and coordination, such as the Bayley-III scale or the Touwen Infant Neurological Examination for infants and toddlers, and the Bruininks-Oseretsky Test of Motor Proficiency, the Visual Motor Integration Test or the Movement Assessment Battery for Children-2 (MABC-2) for school-aged children, among others.

Recent studies have shown that the Bayley scale is one of the best tools for the assessment of infants and young children, while the MABC-2 and the Bruininks-Oseretsky Test of Motor Proficiency would be the preferred assessment tools in school-aged children.9 Stabilometry, also known as posturography, is currently the gold standard for the specific assessment of balance.10

We designed this study with the aim of analysing coordination and balance in school-aged children born preterm with no significant neurological sequelae, comparing them with healthy children born to term of the same age to assess the potential association of the degree of prematurity and these two motor skills.

We conducted a cross-sectional analytical case–control study in children aged 7–10 years born in our hospital between 2001 and 2004. We collected the data for the study in 2012. There were two groups of children under study:

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  Experimental group of children born preterm (≤37 weeks’ gestation). This group was further subdivided based on birth weight into children with birth weights of 1500g or less and with birth weights greater than 1500g. Chronological age was corrected based on 40 weeks’ gestational age.

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  Control group (friends of the children in the experimental group): healthy children born at term (≥37 weeks’ gestation) with adequate birth weights (≥2500g).

We obtained the neonatal and perinatal data of the children born preterm from the database of the neonatal unit, and the information on the control group from structured interviews with the families. We verified that participants in both groups had good clinical outcomes, excluding children with cerebral palsy, chromosomal disorders, muscular disorders, cognitive impairment or severe neurosensory deficits. The sex distribution was random.

The study was approved by the Ethics Committee of the research centre, and the confidentiality of participants was protected conforming to the Declaration of Helsinki of 2008. We obtained the informed consent of the family or legal guardians for all participants in the study.

Movement Assessment Battery for Children-2

We administered the battery of tests corresponding to age band 2 in the MABC-2, which comprehends ages 7 through 10 years.11 This battery assesses three motor skill categories: manual dexterity, aiming and catching, and balance through the performance of eight tasks: placing pegs in a board with holes, threading lace in the holes of a board, drawing a trail, ball throwing and catching, throwing a beanbag aiming at a target, balancing on one foot on a structure that is narrower at the bottom, heel-to-toe walking and hopping on one foot (Fig. 1). The scores obtained in each task are compared with the reference values for each age group to calculate a standard score that ranges between 1 and 19 and a corresponding percentile that is higher the higher the standard score. The sum of the score obtained in the three categories gives rise to a total test score (TTS). Total tests scores greater than 67 or percentiles greater than 15 are considered normal; TTSs ranging from 57 to 67, both included, or percentiles ranging from 6 to 15 indicate risk; and TTSs of 56 or less or percentiles of 5 or less are considered pathological. The interpretation of percentiles is equivalent for each of the three specific categories.

Figure 1.

Exercises performed in age band 2 of the Movement Assessment Battery for Children-2.

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Stabilometry

Postural sway was measured using the Metitur Good Balance force platform and the software GB 300.1.3.20. The test was performed by having the child stand barefoot on the platform with arms lying straight at the sides of the body, with the palms of the hands resting against the outer thighs and the head facing forward in the direction of a mark on the wall placed at the child's eye level. We assessed static postural balance under eight conditions, combining feet together (ft) and feet apart (fa), eyes open (EO) and eyes closed (EC), with and without dampening of proprioceptive input through the addition of foam to the support surface (Fig. 2). Each task lasted 20s. We analysed the following variables: movement velocity (area drawn by the centre of pressure over a predetermined time span [mm2/s]) and length (in mm) of the smallest possible square containing 90% of the force points measured over 20s with a sampling frequency of 100Hz (side length/radius); therefore, lower scores in these variables corresponded to better results.

Figure 2.

Assessment of static balance with feet apart and feet together without foam, and feet apart and feet together with foam using the Metitur Good Balance force platform.

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There is evidence that many of the children born preterm that we considered to be free of neurologic sequelae are at higher risk of developing coordination or balance disorders during school years.2,12–14 This type of disorders could impact numerous activities in the child that are important in developing autonomy, participating in sports, social skills and even academic performance.2,12,15

The MABC has proven to be an effective tool for the detection of coordination disorders in children born preterm. Its latest version, the MABC-2,11 has been validated recently for use in the Spanish paediatric population.16 Still, there is no data on its use on at-risk populations such as children born preterm.

In our study, the prevalence of coordinator disorders in the experimental group of children born preterm using percentiles of 15 or less in the MABC-2 as the cutoff was 15% (birth weight ≤1500g, 13%; birth weight >1500g, and 17%), compared to 13% in the control group; we did not find any differences between groups taking into account the degree of prematurity.

Studies similar to the one we have conducted have found prevalences of approximately 20%,2,15,17 however, a case series of 221 children born with weights of 1500g or less and/or at 32 WG or less18 found a prevalence of 15% at ages 7 and 8 years using the same cut-off point in the MABC, which is consistent with what we found in our series.

There is evidence that the prevalence of this type of disorders is inversely correlated with gestational age and birth weight, as studies conducted in children born preterm with birth weights of 1000g or less and/or at 28 WG or earlier have reported prevalences of about 30–40%3,19,20 and even higher.21

Leaving aside the limitations involved in having a small sample size, we did not find statistically significant differences in the total MABC-2 score within our sample using birth weight as the criterion for determining the degree of prematurity. However, when we categorised the degree of prematurity based on WG, children born at ≤32 WG or less had significantly lower standard scores compared to preterm children born at greater gestational ages.

Part of the variability in the prevalences reported in the literature may stem not only from the degree of prematurity, but also from the age at the time of assessment, the cut-off points used, or the version of the battery, as the scoring and interpretation schemes of the first and second version of the MABC are different and therefore may not be equivalent for the purpose of comparing studies that use different versions.20,22 On the other hand, some studies include children with neurologic sequelae such as cerebral palsy or neurosensory deficits, and this would alter the results to some extent,13,17,22–24 since were the children with neurologic disease excluded from the analysis the results could be comparable to those of the control group, as observed in our study.

Several authors have found that some variables, such as bronchopulmonary dysplasia or retinopathy and especially the presence of white matter lesions in the brain, can impact motor skills test results and the motor competence prognosis of children born preterm,23,25–27 while other variables, such as the early detection and treatment of neurologic sequelae by early intervention teams, could significantly improve motor competence. In our study, 40% of children born preterm with weights of 1500g or less and 10% of those born with weights ranging between 1501 and 2.499g had received this type of treatment, yet we were unable to find evidence of the influence of this variable based on the MABC-2 scores.

However, while some studies show a potential catch-up effect in motor skills scores in children born preterm with no medical comorbidities,19,28,29 others found that even in the absence of medical comorbidities, preterm children could experience greater difficulties performing tasks that require visual-motor integration, manual dexterity or balance,2,23,30 similar to what we found in our case series. Thus, there seems to be a multifactorial mechanism in the motor development of children born preterm.

When it came to the results for the different subscales of the MABC-2 in our study, 37% of children born preterm (birth weight ≤1500g, 27%; birth weight >1500g, 48%) scored in the 15th percentile or lower in the manual dexterity subscale compared to 23% of controls. The total scores in this subscale were significantly lower in the preterm group overall and also in the subgroup of preterm children born at 32 weeks’ gestational age or earlier compared to the control group, so these results suggest that prematurity overall and low gestational age in particular could be risk factors for future manual dexterity difficulties.

We did not find statistically significant differences in aiming and catching, while the total scores in the balance subscale of the MABC-2 were significantly lower in the experimental group of children born preterm and independent of the degree of prematurity. These results are consistent with the literature. Brown et al.20 observed that children with birth weights of 1000g or less had greater difficulties with balance, followed by manual dexterity and last of all aiming and catching using the MABC-2, which was similar to the findings of Zwicker et al25 using the first version of the MABC.

Several studies have shown that children born preterm, including those free of neurologic sequelae, have poorer balance based on some of the tests included in batteries such as the MABC-2 or the Bruininks-Oseretsky Test of Motor Proficiency.2,20,25,27 However, we did not find statistically significant differences between groups using stabilometry, which is considered the gold standard for the assessment of balance10; in fact, in our series, children born preterm occasionally performed better under some of the conditions under study. The observed discrepancies between the two balance assessment tools (MABC-2 and stabilometry) stem from the type of movement that is analysed, as stabilometry specifically assesses postural control and the adaptive response to various controlled changes in sensory input, whereas the MABC-2 includes less specific exercises that involve not only posture control, but other variables such as agility.

Very few studies have used stabilometry in the assessment of children born preterm.26,27,31–33 Kluenter et al.32 assessed balance by means of the Balance Master® platform (NeuroCom; Clackamas, Oregon, USA) in 44 children aged 7 years that had been born preterm with birth weights of 1500g or less and two control groups: healthy children born at term (n=21) and 19 adults; while Lorefice et al.33 used the Wii Balance Master with the LabVIEW software (National Instruments; Austin, Texas, USA) in children born before 30 weeks’ gestation without neurological sequelae at ages 4–5 years (n=90), comparing them with a control group of children born to term (n=36). Both studies had results similar to ours that were not affected by the degree of prematurity.

In the group of children born preterm in our series, despite them being considered free of neurologic sequelae, 15% may have coordination problems or be at risk of developing them based on the assessment with the MABC-2; and even in the group of children that were born at term, approximately 10% may have this type of disorders. Although visual-motor integration was similar in both groups, children born preterm, especially those with higher degrees of prematurity, may experience greater difficulty in the development of fine motor skills, while in the absence of neurologic comorbidities, the balance at ages 7–10 years in children born preterm was comparable to that of healthy children born to term when assessed by means of stabilometry.

This study is part of a project that has been awarded one of the XIV grants for clinical and epidemiological research of the Fundación Ernesto Sánchez Villares in year 2011.

The authors have no conflict of interests to declare.