Infants born weighing less than 1000 g are classified as having extremely low birth weight (ELBW), which continues to be associated with a risk of later neurodevelopmental delay.1,2 Most studies addressing motor performances of infants with ELBW, however, use a total cohort including those with adverse outcomes and those who are apparently nondisabled. There is little information about children who are nondisabled where the association between perinatal risk factors and motor performance during early childhood has been explored.
A range of perinatal variables has been associated with poor developmental outcomes in infants with low birth weight.3–7 For example, using the Griffiths Development Scales, infants with very low birth weight and necrotizing enterocolitis (NEC) at 1 year were found to have impairment in locomotor function compared with those without NEC.3 In addition, higher grades of intraventricular hemorrhage, bronchopulmonary dysplasia, and periventricular leukomalacia (PVL) have been reported to be associated at 18 months with a low psychomotor developmental index on the Bayley Scales of Infant Development in infants with ELBW.6 Similar findings from another study were reported, with sepsis and male gender identified as additional risk factors for having a low psychomotor developmental index between 18 and 22 months.7 Poor locomotor and visual-motor integration functions at 4 years were also identified in Infants with ELBW compared with term peers, using the Griffiths Development Scales.4 In addition, male gender, multiple birth, prolonged mechanical ventilation, and cerebral ventricular dilatation have been found to be independently associated with severe disability at 4 years in children with ELBW.5 Therefore, although studies support the link between some perinatal variables and poorer outcomes in total cohorts of infants with ELBW, little is known of their effect on those infants with ELBW who have no apparent major motor impairment.
The Neurosensory Motor Development Assessment (NSMDA) was developed to measure the quality of children's neuromotor performance against age appropriate reference standards.8 As a criterion-referenced test, the NSMDA differentiates between children with normal and abnormal motor development. It is a valid and reliable instrument and has been used to evaluate the developmental milestones of preterm infants over time.9 Spittle et al10 suggested that the NSMDA was one of the best tests to discriminate between children with normal, minimal dysfunction, mild problems, moderate disability, and severe disability.
The present study aimed to identify the relationship between perinatal risk factors and motor performance as assessed by the NSMDA at age 1 and 4 years corrected for prematurity, and to report the motor outcome changes over time in children with ELBW who were nondisabled.
This study is a retrospective study of longitudinal follow-up data. Ethical approval was obtained from the University and Hospital Institutional Review Boards. Written informed consent forms were obtained from parents.
Infants who were born with ELBW (<1000 g) between 1992 and 1994 and who lived within 250 km of the testing center were included. Those excluded from this study were children diagnosed with neurological impairment such as cerebral palsy or having a General Cognitive Index greater than 2 SD below the mean on the McCarthy Scales11 at 4 years corrected age. A larger study of motor performance and physical fitness in infants with ELBW at 11 to 13 years12 included 105 children with ELBW who fulfilled these criteria. The present study used this cohort in the assessment of motor performances at 1 and 4 years corrected age. Of the 105 Infants with ELBW eligible for inclusion, 57 were lost to follow-up or unavailable to participate in this study, leaving 48 children. Two children did not attend the 1-year follow-up and 2 did not attend the 4-year follow-up. The study group included only children with complete data sets at 1 and 4 years corrected age.
Data for a range of variables previously identified in the literature were extracted from hospital files. Chronic lung disease (CLD) of prematurity was defined as infants who were oxygen dependent at a corrected age of 36 weeks' gestation.13 Other perinatal variables included were multiple birth, gestation, birth weight, gender, prolonged rupture of the membranes, preeclampsia, antepartum hemorrhage, antenatal steroids, Cesarean section, Apgar score at 1 minute, respiratory distress syndrome, patent ductus arteriosus (PDA), NEC grade 2A/3B,14 intracranial hemorrhage grade 3 to 4,15 PVL, retinopathy of prematurity, and sepsis.
Motor performance at 1 and 4 years corrected age were measured using the NSMDA.16 The NSMDA is a standardized test for children from birth to 6 years, used to examine the full range of neurodevelopmental performance, including neurological patterns of movement of infants born premature, sensory-motor function, posture and balance, and gross and fine motor performance. It classifies the children's motor development as within normal range or having minimal, mild, moderate, severe, or profound motor problems and is widely used in Australia and in other countries, particularly for follow-up in premature and low birth weight populations.10,17,18 Children were routinely assessed at these ages (1 and 4 years) by a physiotherapist who was unaware of the child's medical or developmental history as a part of ongoing research and follow-up.
In the NSMDA, the same areas are assessed at each age but the actual tasks included differ, as they are age referenced. At 1 year, the NSMDA test included gross motor items of basic posture in supine and prone, sitting from lying, sitting, rolling, crawling, creeping, cruising along furniture, ability to walk 6 steps without support and the quality of gait. Fine motor aspects include the ability to grasp small beads, type of grasp, ability to manipulate a toy, and awareness of 2 hands in play. Neurological aspects of the test included muscle tone during quiet activity, deep tendon reflexes, clonus, and tremor. Evidence of persisting infant patterns of movement such as hand and foot grasp, galant, extensor thrust reflexes, or labyrinthine and neck postural patterns were noted. The postural/balance aspect included placing and supporting, head righting with respect to gravity, and protective/parachute reactions. The sensory motor aspects included response to touch (upper and lower limbs), eye follow, locating and following a small ball at 1.5 to 2.0 m, and a postrotatory vestibular response.
At 4 years, the gross motor aspects included sitting, quality of gait and walking, ability to stand on 1 leg, ability to walk along a line, hopping, jumping with 2 ft together, and proficiency in catching a ball with both hands. Fine motor aspects included quality and type of pencil grasp and control, and ability to thread 5 beads in less than 30 seconds. Neurological tests were the same at 1 year. The postural/balance aspects were also the same at 1 year, with the addition of testing the child's balance in sitting and standing. The sensory-motor aspects included locating an unseen touch on the face, upper and lower limbs, ability to follow moving objects visually (monocular and binocular), ability to copy demonstrated arm and hand positions, and postrotatory vestibular responses.
For this study, children scored as normal by the NSMDA were allocated to normal category and all others to the abnormal category.
Data were analyzed using SPSS version 18. The distribution of the data was explored, and appropriate statistical analyses were used. To explore the association between perinatal variables and NSMDA scores, motor outcome was categorized as normal (NSMDA scored as normal) or abnormal (NSMDA scored as minimal, mild, moderate). The chi-square or Fisher exact tests were used as appropriate to analyze categorical data, and the Mann Whitney test was used to analyze other nonparametric data. Preliminary analyses were conducted to ensure no violation of the assumption of normality, linearity, multicollinearity, and homoscedasticity occurred before performing regression analysis. Perinatal variables identified from the univariate analysis were entered into the logistic regression model. To explore changes in performance category between 1 and 4 years corrected for prematurity, all changes in NSMDA categories (normal, minimal, mild, moderate) from 1 year to 4 years were explored using the McNemar test. The level of significance was set at α < .05.
Forty-eight children including 27 (56.2%) boys were tested at a mean (SD) age of 53 (3.0) weeks and 4.4 (.4) years. The mean (SD) gestational age of the participants in the study was 27 (2.0) weeks, and the mean birth weight was 784.2 (146.9) g. The perinatal characteristics of participants are presented in Table 1. Differences between the perinatal variables of the 48 participants and 57 nonparticipants (who were lost to follow-up) were evaluated and showed no significant differences between the groups for gender (P = .11), birth weight (P = .15), gestational age (P = .41), CLD (P = .5), and PVL (P = .46).
The motor performances at 1 year and 4 years with respect to the NSMDA results are shown in Table 2. Of note, no child had severe impairment on the NSMDA.
Relationship Between Perinatal Variables and Motor Performance at 1-Year Corrected Age
Results of univariate analyses of perinatal variables by NSMDA categories at 1 year are presented in Table 3. More children with a history of CLD, PDA, and NEC were found in the abnormal NSMDA category at 1 year. In the logistic regression analysis (Table 4), CLD and NEC were found to predict motor performance at 1 year with odds ratio of 14.96 and 20.4, respectively.
Relationship Between Perinatal Variables and Motor Performance at 4 Years Corrected Age
The univariate analyses of perinatal variables by NSMDA categories at 4 years are presented in Table 5. A history of CLD and NEC as well as male gender were found to be associated with an abnormal NSMDA score. In the logistic regression analysis (Table 6), none of the perinatal variables were found to predict motor outcome although there was a trend for an association between CLD and abnormal NSMDA scores (odds ratios: 4.3; 95% confidence intervals: 0.99–18.6).
Changes in NSMDA Category From 1 to 4 Years Corrected Age
No significant changes in allocation to these categories were found from 1 to 4 years (P = .14). Children were allocated to 4 of the 5 categories of NSMDA (no severe motor problems were found). A total of 4 categories are provided in the NSMDA at 1 year, with 54% of the participants remaining in the same classification at 4 years of age. Three of the participants classified as having minimal motor problems at 1 year improved to the normal category at 4 years. Nine of the participants identified as normal at 1 year were found to have minimal motor problems at 4 years. Two of the participants allocated to the moderate category at 1 year improved to the mild problems category at 4 years.
This study appears to be the first to explore the relationship between perinatal variables and motor performance of nondisabled children with ELBW at 1 and 4 years corrected age. Children with ELBW with a history of CLD and NEC were found on multiple regression analysis to have poorer motor performance at 1 year than those free of these conditions. By 4 years, no variables were significant though a strong trend for CLD was found. In this study, CLD and NEC were found to predict motor performance at 1 year.
Although studies of larger cohorts of infants born preterm and/or with low birth weight have shown that CLD was a major factor associated with poor outcome,6,7,19 we found that the children with ELBW who were nondisabled with a history of CLD are still at risk of having poor motor performance in the absence of overt neurological dysfunction. A range of effects have been identified in children with CLD including hypoxia, interruption of lung tissue development, poor nutrition and growth, infection and prolonged hospitalization, and poorer outcome.19,20
Other information also supports the importance of providing timely intervention for the motor problems in this group of children.21 Increasing evidence regarding the poor long-term developmental outcome at school age indicates that even minor motor dysfunction not only relates to 1 domain but also has wider effects on other domains including learning and psychosocial adjustment.22 Identifying those with CLD as “at risk” for motor impairment suggests that physical therapy should be provided as early as possible to minimize the possible motor effects.
The impairment in motor performance at 1 year in the children with ELBW who were nondisabled was predicted by NEC, and although this was still significant on univariate analysis at 4 years, it was not sustained as a predictor. The early effect on motor performance of NEC may be related to gastrointestinal and nutritional problems during the first year of life, which resolved with advancing age. Our study supports the findings of Sonntag et al3 that the effect of NEC on motor development tends to reduce over time. However, advice in handling, positioning, and promoting child activity may facilitate optimal motor gains.
We found no significant changes in the NSMDA category between 1 year and 4 years. The majority of the participants in our study who changed category tended to move 1 level from normal to minimal, or the reverse. These small shifts in performance over 3 years could be expected even in children born at term.
Several researchers have reported a lack of association between social factors and motor outcome,21,23,24 but an association between minor motor difficulties in childhood and ongoing learning and behavioral problems at school age has been reported.22 In addition, the follow-up to age 12 years of the children in the original cohort from which this group was drawn led to a report of poorer than expected motor outcomes,12 so it would seem that the introduction of early physical therapy may be of benefit. Review of the literature supports the importance of reviewing performance around 4 years in children with ELBW who are apparently nondisabled.25 A further benefit would be that proactive movement intervention could then be provided.
Routine follow-up of this cohort occurred as part of the Growth and Development Clinic audit, and these children were not referred for further intervention as no diagnosed impairment or abnormality was identified.12,26 However, as part of their follow-up, parents received general advice about optimizing their child's development.
A limitation of the present study is the relatively small number of participants included. While no statistical differences were found when comparing the characteristics of participants and nonparticipants, we cannot assume that their later motor performance would be similar.
The results of this study indicate that children with ELBW who are nondisabled but with a history of CLD are at risk of having minor motor problems. The importance of the effect of CLD on motor outcomes in early childhood of children with ELBW who are otherwise healthy suggests that careful screening of these children is crucial to identify minor motor difficulties. Thus, specific and objective programs of physical therapy intervention could be introduced on the basis of their specific motor performance and overall development.
The authors thank Kristen Gibbons, Mater Medical Research Institute, for providing statistical advice.
1. Doyle LW, Roberts G, Anderson PJ; Victorian Infant Collaborative Study Group. Changing long-term outcomes for infants 500-999 g birth weight in Victoria, 1979–2005. Arch Dis Child Fetal Neonatal Ed. 2011;96:F443–F447.
2. Mercier CE, Dunn MS, Ferrelli KR, Howard DB, Soll RF; Vermont Oxford Network ELBW Infant Follow-Up Study Group. Neurodevelopmental outcome of extremely low birth weight infants from the Vermont Oxford network: 1998–2003. Neonatology. 2010;97:329–338.
3. Sonntag J, Grimmer I, Scholz T, Metze B, Wit J, Obladen M. Growth and neurodevelopmental outcome of very low birthweight infants with necrotizing enterocolitis. Acta Paediatr. 2000;89:528–532.
4. Stjernqvist K, Svenningsen NW. Extremely low-birth-weight infants less than 901 g: development and behaviour after 4 years of life. Acta Paediatr. 1995;84:500–506.
5. Tudehope DI, Burns YR, Gray PH, Mohay HA, Ocallaghan MJ, Rogers YM. Changing patterns of survival and outcome at 4 years of children who weighed 500-999 g at birth. J Paediatr Child Health. 1995;31:451–456.
6. Ambalavanan N, Nelson KG, Alexander G, Johnson SE, Biasini F, Carlo WA. Prediction of neurologic morbidity in extremely low birth weight infants. J Perinatol. 2000;20:496–503.
7. Vohr BR, Wright LL, Poole WK, McDonald SA. Neurodevelopmental outcomes of extremely low birth weight infants <32 weeks' gestation between 1993 and 1998. Pediatrics. 2005;116:635–643.
8. Burns YR. Physiotherapy Assessment for Infants & Young Children. Brisbane, Queensland, Australia: Copyright Publishing Co Pty Ltd; 1992.
9. Burns YR, O'Callaghan M, Tudehope DI. Early identification of cerebral palsy in high-risk infants. J Paediatr Child Health. 1989;25:215–219.
10. Spittle AJ, Doyle LW, Boyd RN. A systematic review of the clinimetric properties of neuromotor assessments for preterm infants during the first year of life. Dev Med Child Neurol. 2008;50:254–266.
11. McCarthy D. McCarthy Scales of Children's Abilities. New York, NY: The Psychological Corporation; 1972.
12. Burns YR, Danks M, O'Callaghan MJ, et al. Motor coordination difficulties and physical fitness of extremely-low-birthweight children. Dev Med Child Neurol. 2009;51:136–142.
13. Shennan AT, Dunn MS, Ohlsson A, Lennox K, Hoskins EM. Abnormal pulmonary outcomes in premature infants: prediction from oxygen requirement in the neonatal period. Pediatrics. 1988;82:527–532.
14. Bell MJ, Ternberg JL, Feigin RD, et al. Neonatal necrotizing enterocolitis. Therapeutic decisions based upon clinical staging. Ann Surg. 1978;187:1–7.
15. Papile L, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr. 1978;92:529–534.
16. Burns YR, Ensbey RM, Norrie M. The neuro-sensory motor developmental assessment, part 1: development and administration of the test. Aus J Physiother. 1989;35:141–157.
17. Burns Y, O'Callaghan M, McDonell B, Rogers Y. Movement and motor development in ELBW infants at 1 year is related to cognitive and motor abilities at 4 years. Early Hum Dev. 2004;80:19–29.
18. Spittle AJ, Boyd RN, Inder TE, Doyle LW. Predicting motor development in very preterm infants at 1 year' corrected age: the role of qualitative magnetic resonance imaging and general movements assessments. Pediatrics. 2009;123:512–517.
19. Gray PH, Burns YR, Ocallaghan MJ, Tudehope DI, Mohay HA. Neurodevelopmental outcome of preterm infants with bronchopulmonary dysplasia. Arch Dis Child. 1995;73:F128–F134.
20. Narendran V, Donovan EF, Hoath SB, Akinbi HT, Steichen JJ, Jobe AH. Early bubble CPAP and outcomes in ELBW preterm infants. J Perinatol. 2003;23:195–199.
21. Goyen TA, Lui K. Developmental coordination disorder in “apparently normal” schoolchildren born extremely preterm. Arch Dis Child. 2009;94:298–302.
22. Dewey D, Kaplan BJ, Crawford SG, Wilson BN. Developmental coordination disorder: associated problems in attention, learning, and psychosocial adjustment. Hum Mov Sci. 2002;21:905–918.
23. Piek JP, Dawson L, Smith LM, Gasson N. The role of early fine and gross motor development on later motor and cognitive ability. Hum Mov Sci. 2008;27:668–681.
24. Whitaker AH, Feldman JF, Lorenz JM, et al. Motor and cognitive outcomes in nondisabled low-birth-weight adolescents: early determinants. Arch Pediat Adol Med. 2006;160:1040–1046.
25. Caravale B, Tozzi C, Albino G, Vicari S. Cognitive development in low risk preterm infants at 3-4 years of life. Arch Dis Child Fetal Neonatal Ed. 2005;90:F474–F479.
26. Zanudin A, Gray PH, Burns Y, Danks M, Watter P, Poulsen L. Perinatal factors in non-disabled ELBW school children and later performance. J Pediatr Child Health. In press.
brain/growth and development; bronchopulmonary dysplasia; child; child development/physiology; extremely low birth weight infant/growth and development; female; follow-up study; human; male; necrotizing enterocolitis; newborn infant; patent ductus arteriosus; premature infant; psychomotor performance; outcome assessment© 2013 Lippincott Williams & Wilkins, Inc.