Snider, Laurie OT, PhD; Majnemer, Annette OT, PhD; Mazer, Barbara PhD; Campbell, Suzann PT, PhD; Bos, Arend F. MD, PhD
It is well established that infants exposed early to the extrauterine environment are at increased risk for neurodevelopmental impairment and subsequent disability; the incidence increases as birth weight and gestational age decrease.1 Those who initially appear to be developing along a typical trajectory may experience later challenges in more complex tasks,2 specifically in functional everyday activities within home, school, and community environments.3 Early identification is, therefore, essential in the determination of neurological integrity and the potential risk for these sequelae so that early preventive intervention is initiated.4 The question arises as to which approaches to infant assessment are best suited for the early detection of these later outcomes.
Function is the child’s ability to carry out day-to-day tasks and activities according to age expectations.5 The construct of function addresses the child’s ability to perform within the context of environmental demands, not only at the level of impairments (body functions and structures) but in the multidimensional relationship between activities (eg, self care, mobility, domestic life, communication) and participation in daily life (eg, community, social, civic life).6 Functional ability becomes more complex with intrinsic maturation and exposure to environmental experiences. Although developmental outcome measures (eg, Griffiths7) provide a measure of capacity, ie, what the child “can do,” assessments of function measure what the child “does do” within his natural environment.8 Therefore, functional outcome measures may provide a more comprehensive summary of ability than the developmental tests, which have been traditionally used.9
This research article was part of a prospective study, which examined motor and functional outcomes in a cohort of infants born preterm who were assessed at 3 early age points: 34 weeks postconceptional age (PCA), term (38–40 weeks PCA) and 12 weeks adjusted age (AA), and then followed at 1 year of age. This manuscript reports on the results of the assessment at term and the follow-up assessment at 12 months AA, a typical time of neonatal follow-up assessment.
Typically, clinical assessment at term consists of a traditional neurological exam, which is used to evaluate the intactness of the infant’s nervous system, and can include standardized neuromotor or neurobehavioral assessments. The seminal work of Als10,11 has inspired a large body of work, which examines the behavioral interactions of infants born preterm with the environment.12,13 The Assessment of Preterm Infant Behavior,14 a neurobehavioral assessment with established interrater reliability, concurrent and construct validity15 was not a feasible choice for this study because of the extensive training required for examiners. A comprehensive review of the literature found 3 reliable and well validated infant measures representing different contemporary approaches which are suited to the assessment of the infant born preterm at term.16 These were the General Movements Assessment (GMsA),17 the Einstein Neonatal Neurobehavioral Assessment Scale (ENNAS),18 and the Test of Infant Motor Performance (TIMP).19
The GMsA is a qualitative method to detect early central nervous system dysfunction. Its noninvasive nature makes it an important tool in the assessment of fragile neonates. Observations of the quality of endogenously generated “general movements” (GMs) are made to determine the integrity of the infant nervous system. Carried out through serial videotaped observations, a visual gestalt perception technique is used to judge the quality of GMs according to specific criteria.17 The presence of abnormal GMs during repeated tests up to 3 to 4 months of age was found to be more accurate for early identification of infants with neurological deficits than the traditional neurological examination and ultrasound.20 Abnormal GMs were associated with a high risk for cerebral palsy, later minor neurological dysfunction, attention-deficit-hyperactivity disorder, and aggressive behavior at school age.21
The ENNAS is a traditional neurobehavioral assessment which evaluates muscle tone, reflexes, and orienting responses at term and discriminates between high-risk neonates (ie, infants born preterm, small for gestational age, asphyxiated neonates) and healthy infants born full-term. A high false-positive rate is a limitation of this tool.22 To date, the prediction of outcomes for both the GMsA and the ENNAS has been focused on neurologic and cognitive measures rather than functional outcomes.20,22
The TIMP is a functional motor measure designed to evaluate motor control and organization of posture in response to the demands for movement placed on infants by caregivers in naturalistic interactions.22 Specifically, motor behaviors that are relevant to the infant’s day-to-day environmental interactions are evaluated. Studies have shown that the TIMP provides early identification of the delayed development associated with a later diagnosis of cerebral palsy23 and is sensitive to maturational changes in infants born preterm.24 In addition, the TIMP has been used to document treatment outcomes and responsiveness to intervention22 and provides population-based age standards.25 Of the 3 infant measures selected, only the TIMP at 3 months AA has been found to predict functional motor outcomes (ie, mobility) on the Alberta Infant Motor Scales (AIMS) at 12 months AA.26 All 3 share an emphasis on maturational changes in early developmental motor patterns, related to neurological integrity and are used to identify infants at risk. However, it is not evident whether these differing approaches measure similar concepts in different ways.16 Further, none of the 3 measures has been investigated for prediction to functional outcomes at 12 months from assessments performed at term age.
The primary objective of this study was to examine and compare the contributions of 3 different infant assessments of infants born preterm at term: GMsA (neurological); ENNAS (neurobehavioral); TIMP (functional motor) to motor and functional outcomes at 12 months AA. Specifically, we wished to quantify the predictive contributions of the 3 infant assessments, along with known perinatal risk factors, in identifying motor and functional outcomes at 12 months AA in infants who had been born preterm. A secondary objective was to describe the functional abilities at 12 months AA of a representative sample of infants born preterm.
A consecutive series of infants born preterm at or before 32 weeks PCA was recruited from the neonatal intensive care unit (NICU) of a large university hospital and followed prospectively. Weekly medical chart review was conducted by a research coordinator who made telephone contact with eligible families, explained study objectives and procedures and obtained informed written consent before enrollment in the study. The project received scientific and ethical approval from the University and the Hospital institutional review boards.
The goal was to accrue a representative sample of infants born preterm at or before 32 weeks PCA. Infants were excluded if they had a diagnosis of a metabolic disorder, or a cardiac, chromosomal, or congenital abnormality as these represent risk factors for abnormal developmental outcome not specifically related to the motor system.27
Procedures for assessments administered during infancy have been previously reported.16 Briefly, participants were assessed at term age (38–40 weeks PCA) by 2 experienced pediatric occupational therapists, naïve to participants’ history and perinatal course. They were trained in the standardized administration and scoring of the infant assessments (ENNAS, TIMP). Video data for the GMsA were collected continuously during a period of 30 minutes following the morning feeding for all participants. Each participant’s GMsA videotape was sent to be judged by an international expert with extensive training (A.F.B.) who was masked to the history and the results of the ENNAS and TIMP at term. Interrater reliability is established for the GMsA.21,22,28 For the purpose of the study, before the results of the GMsA were known, 10 GMs cases were judged for inter-rater reliability by a coinvestigator (L.S.) trained in the GMsA method, resulting in 100% agreement for normal/abnormal classification (Kappa = 1).29 All examiners were blind to medical history and perinatal course.
Although each of the infant measures was chosen for its excellent reliability,17,22 to provide an estimate of interassessor stability for the purposes of this study, interrater reliability was carried out between the 2 testers for the ENNAS and TIMP on the first 3 consecutive evaluations at the beginning of the study. The primary tester administered and scored the tests and was observed by the second tester who also independently scored the evaluation. The intraclass correlation coefficient (ICC)30 and 95% confidence intervals (CI)30 were calculated for the numerical scores of the tests: (ENNAS: ICC was 0.997 [CI = 0.948–1.00]; TIMP: ICC was 0.856 [CI = 0.540–0.996]), indicating excellent interrater agreement between testers.
Testing at 1 year (12 months AA) coincided with scheduled follow-up clinic appointments. It was carried out by 2 experienced occupational therapists who were different from the testers at term and were masked to the children’s history and the results of the infant assessments. Whereas each of the 4 motor and functional outcome measures administered was chosen for their excellent reliability,22,31–33 to provide an estimate of interassessor stability for the purposes of this study, inter-rater reliability was examined between the 2 testers on the first 3 consecutive evaluations. The primary tester administered and scored the tests and was observed by the second tester who also independently scored the evaluation. ICCs30 and 95% CI30 were calculated for the numerical scores of each of the tests AIMS: ICC was 0.826 (CI = 0.209–0995); Peabody Developmental Motor Scales (PDMS)-2 total score: ICC was 0.992 (CI = 0.886–1.00); Battelle Developmental Inventory (BDI) total score: ICC was 0.815 (CI = 0.242–0.995); Vineland Adaptive Behavior Scales-Daily Living Skills domain (VABS-DLS): ICC was 1.00(CIs were not computed as there was no variation between judges). ICCs were high indicating excellent interrater agreement between testers. CIs were variable because of the small number of cases and the small range of scores.
Perinatal risk factors known to be associated with poor neurodevelopmental prognosis in infants born preterm were collected from the medical record (birth weight, gestational age, presence of intraventricular hemorrhage (IVH), duration of ventilation, and gender34–37).16 The clinical radiologist diagnosed IVH in the presence of hyperechogenicity (ultrasound) in the lateral ventricles and was classified in 4 grades according to Volpe.38
Infant Assessments at Term.
GMs are judged according to Prechtl’s method as normal (N) or abnormal (ABN).17 Those judged as ABN are classified into (1) poor repertoire (PR) or (2) cramped-synchronized (CS).17 At term, predictive abilities similar to those of electroencephalogram (EEG) and neuro-imaging for neurologic and developmental outcome were reported at 18 months of age.21 Predictive validity at 1 year for neurologic examination and the Bayley Scales of Infant Development (BSID)21 was also reported (sensitivity = 80%, specificity = 67%). The quality of GMs between 9- and 16-week AA had a greater specificity for these outcomes compared with GMs findings at earlier ages.21
The ENNAS is comprised of 20 test items and 4 summary items, which evaluate a neurobehavioral repertoire. Items are scored on a 2- to 24-point ordinal scale. Each item has its own scale and is judged as “pass” or “fail” according to a scoring key. Infants are categorized on a total deviant score, equal to the total number of items failed, as normal (<2), suspect (3 to 6), or abnormal (≥7). Psychometric properties and predictive validity are well established.22 Concurrent validity with the neurological examination has been reported (kappa = 0.94, 97% agreement).22
TIMP (Version 5.1)19.
The TIMP consists of 42 items (13 observed and 29 elicited) relevant to infant’s day-to-day environmental interactions. Items measure head orientation, body alignment, distal and antigravity control of leg movements, and auditory and visual responses to stimulation. Each item has its own scale; the number of points varies from 1 to 6. The scores for each item are added to yield a total raw score (maximum 142) and categorized as “average” (+1.0 to −0.5 SD age mean), “low average” (−0.5 to −1.0 SD below age mean), “below average” (−1.0 to −2.0 SD below age mean), “far below average” (>−2.0 below age mean). Criterion content validity studies showed that the TIMP differentiated between the level of maturity (r = 0.83) and the medical risk of the sample (r = 0.85) and that the elicited scale corresponded at 98% with the demands of caregivers.22
Outcome Measures at 12 Months AA
Two measures of motor skill development were used: 1 to evaluate movement quality (AIMS) and 1 to identify the presence of specific gross and fine motor skills ((PDMS-2)).
A norm-referenced assessment of the infant movement repertoire from birth to walking, the AIMS objectively measures motor maturation in children (birth to 14 months). Weight-bearing, posture, and antigravity movements are assessed during spontaneous activity in developmental positions (supine, prone, sit, and standing) and judged according to visual standards. There are 58 items: 21 in prone, 9 in supine, 12 in sitting, and 16 in standing. Each item is scored as either observed (1 point) or not observed (no points). Scores are summed for each position and for the total evaluation to obtain a raw score which is converted to an age-based percentile rank.22 The assessment takes approximately 15 to 30 minutes to administer. Concurrent validity (eg, PDMS, BSID: r = 0.84 to 0.99) and predictive validity at 8 months for pediatrician’s assessment have been established.22 The recommended 5th percentile was used as the cutoff value to categorize participants as either normal or abnormal at 12 months.22 Testing at 1 year can be completed in 20 to 30 minutes.
Normalized most recently in 1997 on a North American sample, this standardized scale is widely used clinically and measures the repertoire of gross and fine motor skills mastered or emerging in children from birth to 5 years. Three composite standard scores are derived (mean = 100; SD = 15): (1) the Gross Motor Quotient (GMQ) consists of 151 items from 4 subtests (reflexes, stationary, locomotion, object manipulation); (2) the Fine Motor Quotient: 98 items from 2 subtests (grasping, visual-motor integration) and (3) the Total Quotient (TMQ): 249 items including all gross and fine motor subtests. The items are scored using a 3-point scale as present,2 emerging,1 not present (0). The maximum raw scores of the subtests are different, ranging from 16 to 198. The Peabody has been used as the gold standard for concurrent validity studies.31,41 With a recommended −1.5 SD cutoff,30 scores below 78 were considered as an indication of delay in each domain. Testing at 1 year can be completed in 25 to 30 minutes.
Assessments of Functional Outcome.
Two functional outcome measures were chosen; one to evaluate developmental and functional repertoire (BDI)32 and specific daily living skills (VABS-DLS).33 Both these measures have been cited as suitable for the assessment of functional outcomes in children born preterm.5,8
BDI, First Edition32.
This standardized assessment battery of the key developmental skills in children from birth to 8 years of age consists of 341 items evaluating 5 domains: personal-social (adult interaction, expression of feelings/affect, self-concept, peer interaction, coping, social role), adaptive (attention, eating, dressing, personal responsibility, toileting), motor (muscle control, body coordination, locomotion, fine motor, perceptual motor), communication (receptive, expressive), and cognitive (perceptual discrimination, memory, reasoning and academic skills, conceptual development). Of these, approximately 82 items lie within the age range of 12 months (personal-social: 19 items; adaptive: 17 items; motor: 29 items; communication: 7 items; cognition: 10 items). This allows for variability of responses among participants and makes the scale responsive to individual differences at this age. Items are scored 2 = always, 1 = sometimes, or 0 = never and responses are summed. Developmental quotients (DQ) (mean = 100, SD = 15) were determined. A recommended −1.5 SD cutoff was used; scores below 78 in each domain indicate delay.32 Testing is conducted through observation and interview and takes approximately 30 minutes to complete.
The VABS is a discriminative, norm-referenced measure which assesses personal and social sufficiency from birth through adulthood. This measure has been used in the literature as a measure of function before 2 years of age in children who are at risk.42 Typical performance in different environments (home, school, community) is evaluated, assessing functional ability and adaptation to everyday demands by means of a semi-structured parent interview. Five domains which can be scored individually are recorded: adaptive, motor skills, communication, socialization, daily living skills (The DLS domain is further comprised of personal, domestic, community subscales: scored adequate, moderately low, or low). For the purposes of this study, only the DLS was administered. Up to 8 items correspond to the abilities of a child at 1 year of age, for example, removes food from spoon with mouth, drinks from a cup (personal subscale), shows understanding that things that are hot are dangerous (community subscale). At 1 year of age, 7 of the 8 applicable items on the DLS are from the Personal subscale, addressing feeding, and the remaining item is from the Community subscale. Items are scored as 2 = yes, usually; 1 = sometimes or partially, 0 = no, never; DK = don’t know; and responses are summed for a total score. Age-based standard scores (mean: 100; SD 15) were used for analysis. A recommended −1.5-SD cutoff was used: scores below 78 were considered as indicative of functional difficulty in the DLS domain.33 Time to complete this subscale was 5 to 10 minutes.
Descriptive statistics, including mean, standard deviation and range were used to characterize the sample for continuous variables (ENNAS, TIMP, total raw or standardized quotient scores on the four 1-year motor and functional outcomes). The sample was further described using the frequencies of categorical scores of the ENNAS and the TIMP as these carry clinical relevance. Frequencies were also calculated for the categorical scores of the GMsA. The categorical scores on the 3 infant tests were then dichotomized into “normal” or “abnormal” using the following classifications: GMsA (normal = N; abnormal = PR + CS); ENNAS (normal = normal + suspect; abnormal = abnormal); and TIMP (normal = average + low average; abnormal = below average + far below average). Classification of each of the continuous results of the 4 motor and functional outcome evaluations were dichotomized as normal or abnormal according to recommended cutoff scores outlined above.
Comparative statistics were carried out. ANOVAs were performed for continuous outcomes and chi square for categorical or dichotomous outcomes, as appropriate. If the results of the ANOVAs were significant, post hoc testing (Dunnett T3) was carried out to determine where the differences lay.
First, the associations between each of the potential explanatory variables (3 infant tests, perinatal risk factors) were studied. At this point, bivariate measures of association between the potential explanatory variables and each of the four 1 year tests were calculated to determine whether there were significant differences in 1-year outcomes (using continuous and dichotomized scores) according to the categorical scores as well as the dichotomized scores of the 3 infant tests. Because all participants were tested within 1 week of their 12-month AA date, raw scores on the BDI were used in the analysis. Multivariate linear regression analyses (continuous outcome scores) and logistic regression models (normal/abnormal outcome scores) were then used to determine the most predictive combination of perinatal risk factors and infant assessments (continuous, categorical, and dichotomous normal/abnormal scores) at term for each of the four 1-year outcomes. A 2-step forward method was used: the first step tested the significance of the perinatal risk factors (ie, potential confounding variables: birth weight, gestational age at birth, presence of IVH, total number of days on ventilation, gender); the second step tested the significance of the infant tests (GMsA, TIMP, ENNAS). To create the most parsimonious model, a variable was retained in the predictive equation if the probability associated with the F value was ≤0.05. Beta values and 95% CI were reported.
A total of 131 families were approached for recruitment during a 2-year period. Of these, 23 declined to participate, resulting in an initial sample of 108. Before the term assessment, a further 8 families withdrew (4 moved, 4 lost to follow-up clinic) leaving a sample of 100 participants at term. The ENNAS, which requires the examiner to rotate the infant through space, was not administered to 5 participants who, because of medical instability, were still attached to monitors at term. The TIMP, which contains some similar elicited items to the ENNAS, was less intrusive overall and thus, was administered to all participants, as was the GMsA. Of the sample at term, 5 of 100 (5%) were unavailable for the 12-month assessment (2 moved, 1 deceased, and 2 lost to follow-up clinic) leaving a final cohort of n = 95. There were no statistically significant differences on any of the perinatal risk factors between those who participated and those who refused. Of the 95 participants seen at 12 months AA, 57.9% (n = 55) were male; 36.8% (n = 35) had birth weights at or below the 10th percentile (mean: 1080 ± 258.5; range 540-1500 g); the range of gestational age at birth was 23.2 to 32.0 weeks (mean: 28.6 ± 2.5 weeks); 26.3% (n = 25) had bronchopulmonary dysplasia (O2 delivered for 28 days or more)37 (mean number of days ventilated: 16.6 ± 21.9; range 0–86 days); and 11.5% (n = 11) had IVH (grade I = 7; grade II = 1; grade III = 2; grade IV = 1).38 Of the 16 participants (16.8%) who had been referred for therapy consultation (12 occupational therapy and 4 physical therapy), 7 had been followed up for intervention (5 occupational therapy and 2 physical therapy), which ranged from monitoring and parent education to treatment once or twice a month.
Performance on Infant Tests and Outcome Measures
Performance on infant tests is presented in Table 1. Table 2 presents the means, standard deviations, and ranges of scores for outcome measures as well as the proportion of participants who scored below the cutoff for each assessment. Results on the AIMS indicated that 66 participants (69.5%) were not walking at 12 months AA; 12 (12.6%) showed early steps, and 17 (17.9%) were walking. Results of the PDMS-2 GMQ locomotion subscale showed that 65 (68%) participants scored below the 25th percentile. With the exception of the adaptive domain, mean scores on all domains of the BDI were below the cutoff score. For VABS-DLS, although no participants were below the cutoff for the total domain score, results on the subscale scores showed a variable performance (personal subscale: adequate = 6 [6.3%], moderately low = 33 [34.7%], low = 56 [58.9%]; domestic subscale: adequate = all [100%]; community subscale: adequate = 22 [23.2%], moderately low = 73 [76.8%]).
Perinatal Risk Factors Associated with Infant Tests
There were no significant differences between classifications of GMsA scores (N, PR, CS) for any perinatal factors. The total number of days on ventilation differed according to ENNAS categories (normal [1.4 days] and suspect [14.4 days]: (Dunnett T3) T = −3.4, p = 0.006). There were significant differences between classifications of TIMP scores for birth weight (low average [x = 1179.8 g] and below average [x = 1008.51 g]: T3 = 2.9, p = 0.032) and for total days on ventilation (the average group [x = 7.1days] and the below average group [x = 23.5 days] were significantly different than the low average group: T = −3.7, p = 0.002 and T = −3.64, p = 0.003, respectively). The “far below average” group showed a higher percentage of participants (57%) with IVH compared with the other TIMP groups (on average 10%) (χ23df = 20.434, p = 0.000). Perinatal risk factors, specifically duration of ventilation, the presence of IVH, and gender were significantly associated with poor motor and functional outcomes at 12 months AA (see Tables 3 and 4). Gestational age was not associated with infant tests.
Prediction of Motor and Functional Outcomes
Measures of Association.
GMsA categories (N, PR, CS) showed a significant association with PDMS-2 GMQ scores below 78 (χ22df = 7.718, p = 0.021) and with walking (no, early steps, yes) on the AIMS standing subscale (χ24dL = 10.669, p = 0.031). The percentage of children not walking at 12 months AA was 60% for category N; 74% for PR, and 100% for CS. Of the children classified as CS, 100% scored below 78 on PDMS-2 GMQ. Dichotomized abnormal GMsA (PR + CS) scores were associated with lower percentile scores on TMQ (F(1,93) = 4.124, p = 0.045) and GMQ (F(1,93) = 4.151, p = 0.044).
Scores on the walking items on the AIMS at 12 months AA differed significantly according to ENNAS categories (normal, suspect, abnormal) (χ24df = 11.162, p = 0.025) (normal = 60%; suspect = 25%; abnormal = 12%).
TIMP category scores (average, low average, below average, far below average) did not show significant associations with any of the four 1-year outcome measures. Dichotomized TIMP scores showed that children with abnormal TIMP scores had lower AIMS performance at 1 year (F(1,93) = 4.316, p = 0.041).
Multiple Linear Regression Analysis.
The significant associations from the multiple linear regression analyses of motor and functional scores are shown in Table 3. The coefficient of multiple determination (R2) indicates the proportion of the variance in the outcome measure explained by the specified infant tests and perinatal risk factors. CI estimate a population value based on what is known about a sample value and are used to estimate a range of values that are likely to include the population mean. If the 95% CI does not cross zero, the results are statistically significant (p < 0.05).
In each of the linear regression models for motor outcomes, only a single variable entered into the model. None of the other variables entered into the model once the first variables were considered. The only variable to enter the multiple linear regression model for the AIMS was the TIMP (continuous score). The regression coefficient was positive indicating that as TIMP scores at term increased, so did AIMS at 1 year. The relation, although significant, was very small; with an r2 of 4.8% (ie, approximately 5% of the variance in AIMS at 1 year of age was explained by TIMP at term).
Results for PDMS-2.
TMQ showed that an abnormal GMsA (PR + CS) accounted for 4.4% of the variance of the percentile score. The negative regression coefficient showed that a child with an abnormal GMsA at term had a lower TMQ score (an average of 5.6 points) than a child who had a normal GMsA. A similar relationship was seen between abnormal GMsA at term and PDMS-2 GMQ percentile score, explaining 4.8% of the variance. Categorical TIMP scores accounted for 4.9% of the variance of the PDMS-2 stationary subscale showing that a child who had a far below or below average TIMP score at term had a stationary percentile score on average 6.3 points less than a child who had an average or low average TIMP at term. The normal/abnormal GMsA score explained 5.0% of the variance for locomotion percentile scores. The negative regression coefficient indicated that a child who had an abnormal GMsA at term had a locomotion percentile score which was on average 8 points less than a child who had a normal GMsA at term. None of the clinical risk variables were associated with the locomotion percentile score. Only the presence of IVH was associated with lower PDMS-2 Fine Motor Quotient scores, explaining 4.3% of the score’s variance. The negative regression coefficient indicated that a child with IVH scored an average of 6.8 points less on Fine Motor Quotient than a child without IVH. Only one clinical risk variable, total number of days on ventilation was associated with lower PDMS-2 grasping percentile score, accounting for 4.5% of the grasping variance. Lower PDMS-2 Visual Motor percentile scores at 1-year AA were associated with presence of IVH, accounting for 7.1% of the score variance.
Clinical risk factors rather than infant tests, explained 5% to 16% of the variance of BDI scores (see Table 3). In most cases, only 1 clinical risk variable entered into the regression model, either duration of ventilation or IVH. However, both duration of ventilation and IVH explained a total of 16% of the BDI communication score. This indicates that for 2 infants with the same duration of ventilation, the one with the IVH would show a BDI communication raw score about 2.8 units less at 12 months AA than the one without IVH.
Logistic Regression Analysis
Table 4 presents the factors significantly associated with each outcome on the logistic regression analyses of categorical scores for motor and functional outcomes.
AIMS scores lower than the 5th percentile were predicted by IVH, gender, and duration of ventilation. The odds ratio for IVH being larger than one, the presence of IVH increased the risk of having an AIMS score below the 5th percentile. The odds ratio for gender being smaller than one, we found that males had a lower risk of scoring below 5th percentile. The odds ratio for duration of ventilation being smaller than one, the longer the ventilation period, the higher the risk for an AIMS score below the 5th percentile. These 3 variables explained 18.3% of the variance. Duration of ventilation was also significant in the prediction of a low score on PDMS-2:TMQ, explaining 5.0% of the variance. The odds ratio being greater than one, the longer the duration of ventilation, the higher the risk of having a score of less than 78.
Two variables predicted a low score on the VABS:DLS total score: the odds ratio being higher than one in both cases, the longer the duration of ventilation, the higher the risk of having a low score. Moreover, this risk was even higher if the participant was male. These 2 variables explained 12% of the variance for this score. The TIMP at term (continuous score) was significant in predicting a low score on the VABS:DLS personal subscale. As the TIMP score at term increased, the risk of having a low score on the personal subscale decreased. No other analyses significantly predicted outcome.
In response to the World Health Organization International Classification of Functioning, Disability and Health (ICF),6 there has been a shift in intervention focus from the impairment level to enhancing function across domains of activities and participation.21 Although developmental outcome measures provide a measure of capacity, the identification of functional deficits in children is important because function identifies the child’s ability to perform within the context of everyday environmental demands. Results of our study show that a large proportion of preterm survivors demonstrated functional delays as measured by the different domains of the BDI (37%–89%). In general, scores on the BDI were low. According to these results, challenges with functional performance appear to originate as early as 12 months AA. Results from the 3 other measures present a more moderate profile: AIMS: 26% of participants scored at or below the 5th percentile cutoff; PDMS-2: 1 to 12% of participants were below the −1.5 SD cutoff; VABS-DLS: no participants scored below the cutoff. The AIMS and PDMS-2 were more comparable in their rate of identification of motor skills, whereas scores on the BDI motor domain seemed to have been much lower. A possible explanation for this finding is that with respect to the BDI, participants were seen at the very beginning of a testing interval (12–18 months) when motor skills are emerging and rapidly differentiating. This may have adversely affected their ability to achieve higher scores on the items presented. Fine motor abilities seem to have presented a greater challenge for a greater proportion of the sample than did gross motor items and these difficulties contributed to the results on the total score on the PDMS-2. Importantly, although participants seemed to be able to meet the demands of the VABS-DLS according to age expectations, in fact, 60% of participants scored “low” on the personal subscale, ie, feeding skills. Based on these findings, intervention to support performance across functional domains (motor, feeding, personal-social, communication, cognitive) should be considered.
Functional motor outcomes pertaining to mobility were predicted by both the GMsA and the TIMP. Only the TIMP predicted functional outcomes in other domains in which 7 of 8 items dealt specifically with feeding skills. As the TIMP was designed to be responsive to postural control, this finding is of interest, considering the postural control required for adequate feeding. The ENNAS was associated with the walking progression on the AIMS but was not predictive of other outcomes at 12 months AA, possibly due to the poor distribution of scores. Perinatal variables of clinical severity, particularly IVH and duration of respiratory support during the NICU hospitalization, accounted for much of the variance in both motor and functional outcome measures. This finding is consistent with previous literature.43 Poor outcome of infants who were ventilated for long periods has been attributed to factors such as sepsis, maternal disease, complications during delivery, and other morbidity factors rather than the actual intervention of ventilation. Infants requiring ventilation were more medically fragile and perhaps more at risk to do less well developmentally over time.37
Assessment at term may be too early for optimal prediction of later performance at 12 months AA. GMsA has been shown to be a better predictor later in infancy (6 to 20 weeks AA) when typically found “fidgety movements” are most prevalent.17 Similarly, data from the administration of the TIMP at 7 days AA showed improved predictive capability at later ages.22 Flegel and Kolobe44also showed that perinatal risk factors were the strongest early predictors of later motor performance and that the TIMP claimed more predictive strength at later ages.
In summary, in 3 different infant tests performed at term, differing aspects of functional gross motor performance were predicted by both the GMsA and the TIMP. Only the TIMP predicted performance in other functional domains. Although these associations were significant, only a small percentage of variance was explained. Further, multivariate analyses showed that perinatal measures of clinical severity accounted for most of the variance in motor and functional outcomes. Therefore, results of infant tests administered at term should be considered in conjunction with biomedical markers of clinical severity. As both GMsA and TIMP have demonstrated improving predictive ability over time, the finding that they appear to predict different aspects of functional performance at term is of ongoing interest. Long-term follow-up of a cohort at preschool age is currently underway to further examine these results. The prevalence of poor functional outcomes in preterm survivors may be due to a combination of motor difficulties, perhaps an over-vigilant style of parents who have been exposed to the insecurities of caring for a fragile preterm infant at home45 or infant challenges in adapting to the home environment.
Our results indicate that, at term, there are multiple factors which may place the infant born preterm at risk for future functional disabilities. On the whole, infant assessments administered at this age appeared to minimally predict motor outcomes and were limited for other functional outcomes. Ongoing follow-up is necessary to ascertain the long-term predictive value of infant assessments for functional outcomes. However, infant assessment at term may be instrumental in ensuring that the infants at most risk for poor outcomes are referred appropriately to early intervention programs which consider the effect of the infant’s environment on function and may improve functional performance.
The authors thank their research assistants (Terry Suss, Antoinette Lemieux, Micah Dear) and occupational therapist evaluators (Sandra Fucile, Claudia DeLuca) for their invaluable contribution to the project. They acknowledge Dr. N. Korner-Bitensky for her review of the manuscript and Dr. J. Lamoureaux for carrying out the statistical analysis. They are indebted to the parents and children who participated in the study. They thank specially Dr. Papageorgiou and Debby Basevitz of the Neonatology Department Jewish General Hospital.
1. Hack M, Horbar JD, Malloy MH, et al. Very low birth weight outcomes of the National Institute of Child Health and Human Development Neonatal Network. Pediatrics
2. Collin MF, Halsey CL, Anderson CL. Emerging developmental sequelae in the “normal” extremely low birth weight infant. Pediatrics
3. Hack M, Taylor HG, Klein N, et al. Functional limitations and special health care needs of 10- to 14-year-old children weighing less than 750 grams at birth. Pediatrics
4. Spittle AJ, Orton J, Doyle LW, et al. Early developmental intervention programs post hospital discharge to prevent motor and cognitive impairments in preterm infants. Cochrane Database Syst Rev
5. Rosenbaum P, Saigal S, Szatmari P, et al. Vineland Adaptive Behavior Scales as a summary of functional outcome of extremely low-birthweight children. Dev Med Child Neurol
7. Griffiths R. The Abilities of Babies
. London: University of London Press; 1954.
8. Ottenbacher KJ, Msall ME, Lyon N, et al. Functional assessment and care of children with neurodevelopmental disabilities. Am J Phys Med Rehabil
9. Rosenbaum P, Stewart D. The World Health Organization International Classification of Functioning, Disability, and Health: a model to guide clinical thinking, practice and research in the field of cerebral palsy. Semin Pediatr Neurol
10. Als H. Toward a synactive theory of development: Promise for the assessment and support of the infant individuality. Infant Ment Health J
11. Als H. A synactive model of neonatal behavioral organization: framework for the assessment of neurobehavioral development in the premature infant and for support of infants and parents in the neonatal intensive care environment. Phys Occup Ther Pediatr
. 1986 6:3–53.
12. Als H, Gilkerson L, Duffy FH, et al. A three-center, randomized, controlled trial of individualized developmental care for very low birth weight preterm infants: medical, neurodevelopmental, parenting, and caregiving effects. J Dev Behav Pediatr
13. Als H, Duffy FH, McAnulty GB, et al. Early experience alters brain function and structure. Pediatrics
14. Als H, Lester BM, Tronick E, et al. Manual for the assessment of preterm infants’ behavior (APIB). In: Fitzgerald H, Lester BM, Yogman MW, eds. Theory and Research in Behavioral Pediatrics
. Vol. 1. New York: Plenum Press; 1982:65–132.
15. Als H, Butler S, Kosta S, et al. The Assessment of Preterm Infants’ Behavior (APIB): furthering the understanding and measurement of neurodevelopmental competence in preterm and full-term infants. Ment Retard Dev Disabil Res Rev
16. Snider L, Majnemer A, Mazer B, et al. A comparison of the general movements assessment with traditional approaches to newborn and infant assessment: concurrent validity. Early Hum Dev
17. Einspieler C, Prechtl HFR, Bos AF, et al. Prechtl’s Method on the Qualitative Assessment of General Movements in Preterm, Term, and Young Infants. Cambridge: MacKeith Press; 2004.
18. Daum C, Grellong B, Kurtzberg D, et al. The Albert Einstein Neonatal Neurobehavioral Scale
. New York: Albert Einstein University; 1977. Located at Unpublished manual.
19. Campbell SK, Osten ET, Kolobe THA, et al. Development of the test of infant motor performance. Phys Med Rehabil Clin North Am
20. Prechtl HF, Einspieler C, Cioni G, et al. An early marker for neurological deficits after perinatal brain lesions. Lancet
21. Palisano RJ, Snider LM, Orlin MN. Recent advances in physical and occupational therapy for children with cerebral palsy. Semin Pediatr Neurol
22. Majnemer A, Snider L. A comparison of developmental assessments of the newborn and young infant. Ment Retard Dev Disabil Res Rev
23. Barbosa VM, Campbell SK, Sheftel D, et al. Longitudinal performance of infants with cerebral palsy on the Test of Infant Motor Performance and on the Alberta Infant Motor Scale. Phys Occup Ther Pediatr
24. Rose R, Westcott S. Responsiveness of the Test of Infant Motor Performance (TIMP) in infants born preterm. Pediatr Phys Ther
25. Campbell S, Levy P, Zawacki L, et al. Population-based age standards for interpreting results on the Test of Motor Infant Performance. Pediatr Phys Ther
26. Campbell SK, Hedeker D. Validity of the Test of Infant Motor Performance for discriminating among infants with varying risk for poor motor outcome. J Pediatr
27. Dusick AM. Medical outcomes in preterm infants. Semin Perinatol
28. Einspieler C, Prechtl HRF, Bos AF, et al. Prechtl’s Method on the Qualitative Assessment of General Movements in Preterm, Term and Young Infants. Cambridge: MacKeith Press; 2004.
29. Cohen J. A coefficient for agreement for nominal scales. Educ Psychol Meas
30. Fleiss J, Cohen J. Reliability of Measurement. In: The Design and Analysis of Clinical Experiments
. New York: John Wiley and Sons; 1986:1–32.
31. Palisano RJ. Neuromotor and Developmental Assessment. In: Wilhelm IJ, ed. Clinics in Physical Therapy: Physical Therapy Assessment in Early Infancy
. New York: Churchill Livingstone Inc; 1993.
32. Newborg J, Stock JR, Wnek L. Battelle Developmental Inventory
. Rolling Meadows, IL: Riverside Publishing; 1984.
33. Sparrow S, Balla D, Cicchetti D. Vineland Adaptive Behavior Scales Interview Edition: Survey-Form Manual
. Circle Pines, MN: American Guidance Service; 1984.
34. Majnemer A, Rosenblatt B, Riley PS. Influence of gestational age, birth weight, and asphyxia on neonatal neurobehavioral performance. Pediatr Neurol
35. Msall ME. The panorama of cerebral palsy after very and extremely preterm birth: evidence and challenges. Clin Perinatol
36. Hintz SR, Kendrick DE, Vohr BR, et al; For the Nichd Neonatal Research N. Gender differences in neurodevelopmental outcomes among extremely preterm, extremely-low-birthweight infants. Acta Paediatrica
37. Gregoire M, Lefebvre F, Glorieux J. Health and developmental outcomes at 18 months in very preterm infants with bronchopulmonary dysplasia. Pediatrics
38. Volpe J. Neurology of the Newborn
. Philadelphia, PA: WB Saunders Company; 2001.
39. Piper MC, Darrah J. Motor Assessment of the Developing Infant
. 1st ed. Philadelphia: WB Saunders Co; 1994.
40. Folio M, Fewell RR. Peabody Developmental Motor Scales Examiner’s Manual
. 2nd ed. Austin, TX: Pro-Ed; 2000.
41. Connolly B, Dalton L, Smith J, et al. Concurrent validity of the Bayley Scales of Infant Development II (BSID-II) Motor Scale and the Peabody Developmental Motor Scale II (PDMS-2) in 12-month-old infants. Pediatr Phys Ther
42. Limperopoulos C, Majnemer A, Shevell MI, et al. Functional limitations in young children with congenital heart defects after cardiac surgery. Pediatrics
43. Bennett FC. Perspective: low birth weight infants: accomplishments, risks, and interventions. Infants Young Child
44. Flegel J, Kolobe TH. Predictive validity of the Test of Infant Motor Performance as measured by the Bruininks-Oseretsky Test of Motor Proficiency at school age. Phys Ther
45. Schenk LK, Kelley JH, Schenk MP. Models of maternal-infant attachment: a role for nurses. Pediatr Nurs
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