Abstract
Background Only a few studies have been conducted with the objective of creating norms of the Alberta Infant Motor Scale (AIMS) for the assessment of gross motor development of preterm infants. The AIMS performance of preterm infants has been compared with that of the Canadian norms of full-term infants, but not with that of full-term infants of the same nationality. Moreover, the possible impact of prematurity-related morbidity factors on AIMS performance is unknown.
Objectives The aims of this study were: (1) to evaluate AIMS trajectory in a large population of Greek preterm infants and create norms, (2) to compare it with the AIMS trajectory of Greek full-term infants, and (3) to examine the possible influence of neonatal morbidity on AIMS scores in the preterm sample.
Design This was a cross-sectional study.
Methods Mean AIMS scores were compared, per month (1–19), between 403 preterm infants (≤32 weeks of age, corrected for prematurity) and 1,038 full-term infants. In preterm infants, the association of AIMS scores with respiratory distress syndrome (RDS), intraventricular hemorrhage (IVH) of grade ≤III, bronchopulmonary dysplasia (BPD), retinopathy of prematurity (ROP), and sepsis was assessed by hierarchical regression analysis.
Results Alberta Infant Motor Scale scores were significantly lower in preterm infants than in full-term infants. Mean AIMS scores in preterm infants were significantly associated with RDS (b=−1.93; 95% CI=−2.70, −1.16), IVH (b=−0.97; 95% CI=−1.69, −0.25), and ROP (b=−1.12; 95% CI=−1.99, −0.24) but not with BPD or sepsis in hierarchical regression analysis.
Conclusions Alberta Infant Motor Scale norms were created for Greek preterm infants. This study confirms that AIMS trajectories of preterm infants are below those of full-term infants of the same nationality. The influence of morbidity factors, including RDS, IVH, and ROP, should be taken into account when administering the AIMS in preterm infants.
Despite the increase in the survival rate of the smaller and more immature infants born preterm with very low birth weight (VLBW) as a result of improvements in perinatal and neonatal care over the past 3 decades,1 the neurodevelopment of these “fragile” babies is still a matter of concern. Health professionals participating in follow-up programs of infants born prematurely pay specific attention to motor development, especially in the first year of life, as it is well known that gross motor development during infancy indicates, at least partly, the integrity and functionality of the central nervous system.2–4
The Alberta Infant Motor Scale (AIMS) is a reliable and easy-to-use clinical assessment tool for the evaluation of infant gross motor development. The AIMS is a norm-referenced test that assesses, via observation, the spontaneous motor performance of infants from birth through independent walking (0–19 months).5 It has been recognized as a useful tool to assess gross motor maturation during infancy, to trace motor delay, and to identify infants who may benefit from early intervention.5,6 The AIMS was initially applied on a Canadian population of infants born full-term as a norm reference test; a recent re-evaluation of the scale showed that the previously reported normative values remain valid 20 years later.7 In addition to its initial application on the Canadian population, the AIMS has been broadly used throughout the world in many studies and in daily clinical practice to evaluate, primarily, the motor development of full-term infants.8–16 The AIMS also has been used to evaluate the motor development of preterm infants, especially in the recent past.17–23
Although the AIMS is largely considered today as a proper tool for the evaluation of preterm infants, only a few studies have been conducted to compare AIMS performance between preterm and full-term infants and to create norms for infants born prematurely.21–23 Indeed, differences in AIMS scores between preterm and full-term infants, at ages corrected for prematurity, have been reported.21–23 A major limitation of those studies was the fact that the preterm infant population was compared with the original Canadian sample of full-term infants but not with full-term infants of the same nationality.21,22 Genetic factors, extreme climates, or potential cross-cultural differences across nationalities might have had an effect on the infants' motor development.24 It was previously reported that common child handling practices in everyday care (ie, holding, dressing, bathing) may influence the onset of infants' motor abilities and their developmental path and outcome.24 Moreover, in a previous study in full-term infants,16 we showed that specific cultural characteristics of Greek society were associated with infant motor development; being raised by grandparents and baby-sitters had a significant effect on the motor development of infants.16 Furthermore, the knowledge of the impact of prematurity-related morbidity factors (ie, respiratory distress syndrome [RDS], intraventricular hemorrhage [IVH], retinopathy of prematurity [ROP], bronchopulmonary dysplasia) on AIMS performance would be useful information to improve AIMS interpretation. Interestingly, although prematurity-related morbidity factors are expected to contribute to performance on the AIMS, in accordance with what is already known about the impact of neonatal morbidity on preterm infant motor development evaluated with assessment tools other than the AIMS, only one small-scale study, to our knowledge, has tried to address this issue; the results were inconclusive due to the small sample.23
The aims of this study were: (1) to compare the AIMS trajectories, from 1 to 19 months of age, between large populations of very preterm (≤32 weeks of gestation) Greek infants and full-term infants of the same nationality, (2) to create AIMS norms for Greek preterm infants to identify (in the future) whether individual preterm infants are not following the expected trajectory, and (3) to evaluate the possible influence of common neonatal morbidity factors on AIMS performance of the preterm infant population.
Method
Sample
The study population consisted of 403 preterm infants and a control sample of 1,038 healthy full-term infants. The age range of the infants studied was 1 to 19 months. Preterm infants born before or at 32 weeks of gestational age, without major morbidity that might have had a severe impact on motor development, were studied. Exclusion criteria included congenital anomalies or syndromic features, severe brain abnormality (periventricular leukomalacia, IVH >III grade, congenital hydrocephalus) or central nervous system infection (encephalitis, meningitis), and necrotizing enterocolitis. In the group of preterm infants, 251 (62.3%) were boys. The mean birth weight was 1,154.0 g (SD=343.9), and the mean gestational age was 28.6 weeks (SD=2.3). Ninety-six (23.8%) of the 403 preterm infants were small for gestational age (birth weight below the 10th percentile).
Among the group of full-term infants, 584 (56.3%) were boys. Mean birth weight was 3,256.6 g (SD=387.3), and mean gestational age was 38.6 weeks (SD=0.4). Criteria for eligibility of full-term infants were reported in our previous study conducted to standardize AIMS in a Greek population of full-term infants.16,25 That study showed that gross motor development of healthy Greek full-term infants, assessed with the AIMS during the first 19 months of age, follows a similar course to that of the original Canadian sample.16 There was no difference between Greek preterm and full-term infants regarding socioeconomic parameters, such as parental age, family educational level, birth order, and number of siblings.
In preterm infants, the influence of the most frequent or most common morbidity factors related to prematurity, including RDS, IVH of grade ≤III, bronchopulmonary dysplasia, ROP, and sepsis, on AIMS performance was assessed. All preterm infants underwent brain ultrasound and ophthalmologic examination routinely during hospitalization. Respiratory distress syndrome was diagnosed following clinical and chest radiographic findings. Preterm infants with RDS were separated into 3 groups, as follows: (1) mild RDS (no need for conventional mechanical ventilation), (2) moderate RDS (need for conventional mechanical ventilation for ≤3 days), and (3) severe RDS (need for conventional mechanical ventilation for >3 days). Intraventricular hemorrhage was classified according to Papile classification. Bronchopulmonary dysplasia was defined as oxygen supplementation required for at least 28 days. Infants with ROP were divided into 2 groups, depending on the grade of retinopathy (ROP <3 and ROP ≥3). With regard to sepsis, only confirmed cases with positive blood cultures were selected.
The recruitment of infants began in January 2009 and was completed in November 2013. Evaluation of interrater reliability among 3 independent examiners, who had received adequate training by the first author (D.S.) prior to the start of the study, was performed in a random sample of 87 participants, as reported in our previous study in full-term infants.25 The full-term sample was derived from maternity and pediatric clinics, public and private day care centers, and private pediatricians' offices located in various areas of the Prefecture of Attica. The preterm infant sample was derived from the follow-up clinics of the Neonatal Unit of the First Department of Pediatrics, Athens University Medical School, and the First Department of Neonatal Intensive Care Unit of Aghia Sophia Children's Hospital, Athens, Greece. The assessment of the infants was performed at home, in maternity and pediatric clinics, and in private pediatricians' offices, but always in the presence of the parents so that the infants could feel secure and relaxed.
The caretakers of the organizations providing input for our research were informed about the aim and method of the study. Parental informed consent also was obtained.
Assessment Tool
The AIMS consists of 58 items at 4 different positions: prone (21 items), supine (9 items), sitting (12 items), and standing (16 items). The components tested for each item are based on 3 elements of movement: weight bearing, posture, and antigravity movements. For any item observed by the examiner, 1 point is given, whereas 0 points are given when the item is not observed. The sum of all items observed gives the total raw score, ranging from 0 to 58. The total raw score also can be converted into a percentile rank. High percentile ranks indicate maturity of the infant's gross motor skills.5,6
Data Analysis
Mean AIMS scores of preterm infants at postnatal age corrected for prematurity were compared with those of full-term infants to identify possible differences in gross motor development between the 2 groups. Comparisons were performed at each age level, from 1 to 19 months, using Student t test. The Kolmogorov-Smirnov test was used to assess normality. In the sample of preterm infants, hierarchical regression analysis was used to test the effects of common morbidity factors related to prematurity (RDS, IVH ≤III grade, bronchopulmonary dysplasia, ROP, sepsis) on total raw AIMS score independently of the influence of other predictors. Five regression analysis models were performed, with total AIMS score as dependent variable and each specific neonatal morbidity factor as independent variable. The neonatal morbidity factors studied could not be included in the same model due to high collinearity. Significance level was set at P≤.05. The data were analyzed using IBM SPSS statistical package, version 19.0 (IBM Corp, Armonk, New York).
Results
The scoring pattern across the 4 subscales of the AIMS (in prone, supine, sitting, and standing positions) for preterm and full-term infants according to monthly age level is shown in Figure 1. In the prone position, the mean AIMS scores were significantly lower in preterm infants than in full-term infants up to the age of 12 to 13 months. In the supine position, differences were recorded up to 8 to 9 months of age, whereas thereafter both curves reached a plateau. In the sitting position, the mean AIMS scores in preterm and full-term infants were quite close during the first months of age, but they differed significantly thereafter at several age levels (at 3–4 months, from 5–6 to 9–10 months, and from 11–12 to 12–13 months). In the standing position, mean AIMS scores were significantly lower in preterm infants than in full-term infants throughout the entire study period from 1 to 2 months of age to 18 to 19 months of age.
Mean values of preterm and full-term infants according to monthly age level for each of the 4 subscales of the Alberta Infant Motor Scale: (A) prone, (B) supine, (C) sitting, and (D) standing.
As a consequence of the above findings in AIMS subscales, total AIMS scores were significantly lower in preterm infants than in full-term infants (P<.0001) (Fig. 2). The difference between groups was significant at each age category (Tab. 1). Even after performing a Bonferroni correction to adjust for multiple comparisons, the differences between preterm and full-term infants remained significant.
Mean total of the Alberta Infant Motor Scale (AIMS) score curves of 403 preterm infants versus the 1,038 full-term infants.
Distribution and Mean (SD) AIMS Scores of Full-term and Preterm Greek Infants According to Monthly Age Level
In preterm infants, the motor developmental pattern did not differ significantly between boys and girls at any monthly age level or in total trajectory from 1 to 19 months. As expected, postnatal age correlated positively with total AIMS score (P<.001). The rate of mean increase in total AIMS score by monthly age level did not differ significantly between preterm infants (3.42 points; 95% confidence interval [CI]=3.27, 3.57) and full-term infants (3.34 points; 95% CI=3.26, 3.43). A negative association between total AIMS score and being born small for gestational age in preterm infants after adjusting for postnatal age also was recorded (P=.03).
The distribution of neonatal morbidity factors in the group of preterm infants is shown in Table 2. After adjustment for postnatal age and being born small for gestational age, 3 neonatal morbidity factors were found to have a small, but statistically significant, negative influence on total AIMS scores in hierarchical regression analysis: RDS, IVH, and ROP (Tab. 3). Specifically, the mean AIMS raw score in preterm infants was decreased by 1.93 (P<.0001), 0.97 (P=.008), and 1.12 (P=.012) points when there was an increase of one level in the severity of RDS, IVH, and ROP, respectively. In all models studied (Tab. 3), postnatal age and being born small for gestational age were recognized as independent predictors of total AIMS scores. Mean total AIMS scores were not found to be associated with bronchopulmonary dysplasia (P=.900), whereas the association with sepsis tended toward, but did not reach, a statistically significant level (P=.075).
Distribution of Neonatal Morbidity Factors in the Group of 403 Preterm Infantsa
Results of Hierarchical Multiple Regression Analysis Showing Changes in AIMS Score by Neonatal Morbidity Factorsa
Discussion
To our knowledge, this is the first study in which AIMS performance of a large cohort of preterm infants was compared with that of a reference sample of full-term infants of the same nationality. All previous relevant studies from other countries, with the exception of one small-scale study,23 compared AIMS scores of preterm infants with Canadian norm-referenced values derived from full-term infants.21,22
The largest previous relevant study was that of van Haastert et al, in 2006, which included 800 Dutch preterm infants, ≤32 weeks of gestational age, between 1 and 18 months of corrected postnatal age.22 Although the number of infants studied was approximately 2 times larger than the number of infants in our study population, the distribution of children per month of evaluation was not normal, with 549 (68.6%) out of 800 infants having been assessed at 2 time points (at 6–7 and 15–16 months of corrected age). Moreover, a number of infants were evaluated with the AIMS more than one time during the 18-month period.22 The authors concluded that gross motor developmental trajectories of preterm infants in the first 18 months of life are lower compared with those in the original Canadian full-term sample.22 In 2010, Kayenne Martins Roberto Formiga and Linhares also found lower AIMS scores, from 1 to 12 months of corrected age, in 308 preterm infants born in Brazil at ≤37 weeks of gestation in comparison with the established Canadian normative sample.21 In that study, preterm infants were evaluated with the AIMS from birth to 12 months, but not thereafter.21 Only in the study by Pin et al, in Australia, was the AIMS performance of preterm infants, <30 weeks of gestation, compared with that of full-term infants of the same nationality.23 The infants were longitudinally assessed at 4, 8, 12, and 18 months of corrected age. The preterm group scored significantly lower at all 4 age levels compared with the group of full-term infants. However, the study population consisted of only 46 preterm and 48 full-term infants, whereas preterm infants with severe morbidity, such as IVH of grade≥III, ventriculoperitoneal shunt insertion, seizures, or necrotizing enterocolitis with abdominal surgery, also were included.
As expected, the results of our study confirm that gross motor mobility, assessed with the AIMS, is indeed inferior in preterm babies than in full-term babies, even after correcting for the degree of prematurity. This finding is further strengthened by the fact that our preterm infants were relatively “healthy,” as we excluded neonatal diseases known to be associated with increased risk for abnormal motor development. Preterm infants scored lower than full-term infants in all 4 AIMS subscales in the prone, supine, sitting, and standing positions. They first reached the full-term score in the supine position and then in the prone and sitting positions, whereas they scored significantly lower in the standing position up to the end of the evaluation period, at 19 months of corrected age. From the above, it seems that preterm babies follow the normal gross motor development of full-term infants, but at a slower pace. We suggest that adjusted AIMS norms ideally should be used for proper evaluation of preterm infants. Whether each country should use AIMS norms derived from its own preterm infant population or whether preterm infant norms from other countries also would be appropriate should be further studied. Otherwise, the original Canadian sample could be used, but preterm infants should be expected to follow at least their own lower percentile rank.
The evaluation of the impact of common medical complications of prematurity on AIMS performance in a large population of preterm infants is also an original aspect of this study. The negative association of neonatal morbidity factors on gross motor development of preterm infants is in accordance with previous studies that did not use Alberta assessment tools.26,27 Although the change in R-square value, a way to evaluate how much predictive power was added to the model, was not large enough by the addition of RDS, IVH of grade ≤III, or ROP (Tab. 3), it was statistically significant. Postnatal age and being born small for gestational age explained the largest percentage of variability in total AIMS scores (Tab. 3).
Bronchopulmonary dysplasia was not found to be significantly associated with the motor outcome of the infants studied. Although it appears in the literature that preterm infants with bronchopulmonary dysplasia are at risk for neurodevelopmental compromise,26 it also has been reported that bronchopulmonary dysplasia is not independently associated with adverse neurodevelopmental outcome, as its association with disability was no longer apparent after adjusting for the presence of other neonatal morbidity factors related to prematurity.28,29 With regard to sepsis, its association with motor development, in our study population, tended toward, but did not reach, a statistically significant level (P=.075). Previous studies have shown that neonatal sepsis has a significant negative impact on neurodevelopment.30,31 The absence of a significant association between sepsis and AIMS scores in our study can possibly be attributed to the small number of infants with sepsis, as only cases of sepsis confirmed by positive blood culture were selected. In addition to morbidity factors found to be associated with AIMS performance, the differences in AIMS scores between our preterm and full-term infants could possibly be attributed to other causes related to hospitalization of preterm babies in neonatal units, such as abnormal position (ie, increased body extension), reduction in movements as a result of mechanical ventilation, invasive procedures, and episodes of pain and stress, which may contribute to altered neurodevelopment.32–34
In conclusion, norms for Greek preterm infants, ≤32 weeks of gestation, using the AIMS, prove that preterm infants exhibit inferior motor trajectories, from 1 to 19 months of corrected age, compared with full-term peers of the same nationality. Thus, adjusted AIMS norms ideally should be used for proper evaluation of preterm infants. It is possible that adjusted norms for the evaluation of preterm infants should be derived from each country's own preterm infant population, but this issue needs to be further studied. The significantly lower gross motor maturity of preterm infants is associated with some neonatal morbidity factors, including RDS, IVH, ROP, and being born small for gestational age. Clinicians should expect that common or mild morbidity during hospitalization in the neonatal intensive care unit may affect motor development of even “healthy” preterm infants. Morbidity factors should be taken into account in decision making for early intervention or physical therapy in these infants.
Footnotes
Mr Syrengelas and Dr Siahanidou provided concept/idea/research design and writing. Mr Syrengelas, Mrs Kleisiouni, Mrs Manta, and Dr Mellos provided data collection. Mr Syrengelas, Mrs Kalampoki, and Dr Siahanidou provided data analysis. Mr Syrengelas provided project management and facilities/equipment. Dr Siahanidou provided participants. Mrs Kleisiouni, Mrs Manta, Dr Mellos, Dr Pons, Dr Chrousos, and Dr Siahanidou provided consultation (including review of manuscript before submission).
The aims and design of the study was approved by the Ethics Committee of Aghia Sophia Children's Hospital.
- Received November 11, 2014.
- Accepted November 22, 2015.
- © 2016 American Physical Therapy Association
References
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