PEDIATRICS Vol. 120 No. 5 November 2007, pp. 1012-1019 (doi:10.1542/peds.2006-3364)
ARTICLE |
Twelve-Month Neurofunctional Assessment and Cognitive Performance at 36 Months of Age in Extremely Low Birth Weight Infants
Neonatal Intensive Care Unit, Institute of Pediatrics and Neonatology, Fondazione IRCCS "Ospedale Maggiore Policlinico, Mangiagalli e Regina Elena" University Medical School, Milan, Italy
 |
ABSTRACT |
|---|
 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSAPPENDIX: NEUROFUNCTIONAL...REFERENCES |
|---|
OBJECTIVE. The objective of this study was to investigate whether an early neurofunctional assessment (at 12 months’ corrected age) is predictive of cognitive outcome at 36 months of age in extremely low birth weight infants.
METHODS. We conducted an observational longitudinal study. Neurodevelopmental outcome by means of a neurofunctional assessment was evaluated at 12 months’ corrected age and 36 months’ chronological age in 141 extremely low birth weight children. Cognitive outcome was assessed with use of the Griffiths Mental Developmental Scale.
RESULTS. A significant association was found between the 12-month neurofunctional status and cognitive performance at 36 months. A higher general quotient on the Griffiths Mental Developmental Scale at 36 months was observed in infants who exhibited normal (score: 
1) neurodevelopment compared with children who exhibited minor (score: 2) and major (score: 
3) dysfunctions at the 12-month neurofunctional evaluation (99 ± 6.8 vs 85.3 ± 16.3 vs 57.3 ± 22.0). A score of 2 at the 12-month neurofunctional assessment, abnormal brain MRI results at term, and chronic lung disease remained predictive of cognitive delay at 36 months of age and also after adjustment for confounders.
CONCLUSIONS. The 12-month neurofunctional evaluation may be an additional useful clinical tool in predicting later cognitive outcome in extremely low birth weight children.
Key Words: neurofunctional assessment • cognitive outcome • extremely low birth weight infants
Abbreviations: VLBW—very low birth weight • ELBW—extremely low birth weight • SGA—small for gestational age • NEC—necrotizing enterocolitis • ROP—retinopathy of prematurity • CLD—chronic lung disease • HC—head circumference • GQ—general quotient
Survival of very low birth weight (VLBW; <1500 g) infants has recently improved as a result of advances in perinatal care.1 Major disabilities occur in 15% to 20% of the VLBW population, with a higher prevalence in infants with the youngest gestational age and the lowest birth weight.2 A high rate of learning difficulties, behavioral problems, and lower IQ scores, compared with the population mean, is reported in survivors without major dysfunctions, especially extremely low birth weight (ELBW; <1000 g) infants.3 Early detection of infants who are at high risk for poor neurodevelopmental outcome remains a challenge for clinicians to make referral for intervention and optimize potential outcome. Several authors4, 5 have investigated the relationship between motor ability, mainly investigated by a developmental assessment of movement, and cognitive performance in ELBW, suggesting that early movement problems may be predictive of later cognitive adverse outcome even in the absence of defined neurologic problems.
We previously reported that an early neurofunctional evaluation in VLBW infants may be an additional useful tool in reassuring parents on the integrity of central nervous system function.6 Few data are available in the literature on any hypothetical relationship between cognitive outcome of ELBW infants and early neurofunctional assessment.7, 8 The aim of this study was to examine whether a neurofunctional evaluation at 12 months is predictive of cognitive outcome at 36 months of age in ELBW infants.
|
METHODS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSAPPENDIX: NEUROFUNCTIONAL...REFERENCES |
|---|
Among all consecutive newborn infants who were admitted at the same Institution from 1996 to 2001, 159 infants entered the study. Inclusion criterion was birth weight
1000 g. Exclusion criteria were presence of congenital diseases and/or chromosomal abnormalities or infant death during postpartum hospital stay. Infants were scheduled to be prospectively followed up to 36 months of age. The Consolidated Standards of Reporting Trials (CONSORT) flowchart of the study is shown in Fig 1. Written informed consent was obtained from the newborns’ parents, and the departmental ethics committee approved the study design.
|
Presence of gestational hypertension and/or preeclampsia, steroids received before delivery, and educational level were investigated as maternal variables. Gestational hypertension and preeclampsia were defined, respectively, as de novo hypertension (systolic blood pressure
140 mmHg or diastolic BP 90 mmHg) arising after midpregnancy and gestational hypertension associated with new-onset proteinuria (300 mg/24 hours). The educational level of mothers was evaluated and categorized as low (13 years) or high (>13 years).
Neonatal characteristics (gestational age, being appropriate or small for gestational age [SGA], birth weight, length, and head circumference); need for mechanical ventilation; and the occurrence of sepsis, necrotizing enterocolitis (NEC; classified as stage 3 according to the classification of Bell et al9), bronchopulmonary dysplasia, and retinopathy of prematurity (ROP) of stage 3 or higher were recorded prospectively. Gestational age was based on the last menstrual period and first-trimester ultrasonogram. Infants with birth weights of 10th or <10th percentile for gestational age, according to the North-Italian growth charts, were classified as appropriate for gestational age or SGA, respectively.10 Sepsis was defined by the presence of a positive blood culture. Patients with NEC were pooled together with those who had sepsis because of the strong association of NEC with infection. Chronic lung disease (CLD) was defined by use of supplemental oxygen at 36 weeks’ postconceptional age. Corrected age was calculated, up to 24 months of life, from the chronologic age adjusting for gestational age. Brain MRI was performed at a mean of 40 ± 2 weeks’ postconceptional age in all newborns. An abnormal MRI result was defined by the presence of major brain lesions (eg, ventriculomegaly, cystic and noncystic periventricular leukomalacia, focal parenchymal brain lesions).
Infants entered a follow-up program that consisted of periodic pediatric visits at 3, 6, 12, and 24 months’ corrected age and 36 months’ chronological age and of evaluation of neurodevelopmental outcome by means of the neurofunctional evaluation at 12 months’ corrected age and 36 months’ chronological age. Cognitive outcome was assessed with use of the Griffiths Mental Developmental Scale at 36 months’ chronological age.
Weight, length, and head circumference (HC) were measured using standardized procedures.11 Growth z scores were then calculated by EuroGrowth 2000 software (EuroGrowth Study Group, Vienna, Austria). Catch-up growth was defined by a growth z score of more than –2 SD.
The neurofunctional evaluation6 was based on the study of evoked and spontaneous motility, postural adaptability, variability of motor patterns, and neuromotor and behavioral skills. A detailed description of the neurofunctional assessment is reported in the Appendix. Infants were categorized into 3 groups, according to the neurofunctional status, as normal (score: 0–1), exhibiting minor dysfunctions (score: 2), or exhibiting major dysfunctions (score: 3–4). The Griffiths Mental Development Scale12 and related subscales (locomotor, personal social, hearing and speech, hand and eye coordination, performance, and practical reasoning) were administered by the same expert trained examiner, who was blind to the neurofunctional evaluation. A general quotient (GQ) was then calculated. The mean value of GQ was 100 with an SD of 12. A GQ of <70 was classified as severe developmental delay.
Statistical Analysis
Descriptive data are shown as means ± SD or number of observations (percentage). Comparison among groups was performed by the 
2 test for discrete variables or by analysis of variance for continuous variables. Significance of multiple comparisons was adjusted by the least significant difference test correction. Differences within patients in repeated measurements of growth parameters were assessed by analysis of variance. Logistic regression analysis was used to identify determinants of developmental delay (GQ < 88) at 36 months of age. Maternal and neonatal characteristics that are known to be associated with adverse cognitive outcome were entered in the model. Factors examined included maternal education, prenatal steroids, maternal hypertension, multiple birth, gender, birth weight, gestational age, being SGA, sepsis, ROP of stage 3 or higher, HC catch-up growth at 12 months, neurofunctional status at 12 months’ corrected age, CLD, and cranial MRI status at term.
All statistical analyses were conducted at the 
= .05 level and were 2-tailed. Statistical analysis was performed by using SPSS 12 (SPSS Inc, Chicago, IL).
|
RESULTS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSAPPENDIX: NEUROFUNCTIONAL...REFERENCES |
|---|
Follow-up data at 36 months’ chronological age were available for 141 (70 girls; 71 boys) infants. One infant died through the follow-up. No differences in the characteristics at birth and in the developmental measures, when last assessed, were observed between infants who were lost at follow-up and those who were evaluated. The characteristics of the studied population at birth are shown in Table 1.
|
Maternal hypertension occurred in 35.1% and 39.4% of mothers with infants who exhibited a GQ of <88 and
88, respectively, at 36 months’ chronological age (P = .39). Antenatal steroids were administrated to 50% and 59.5% of mothers with infants who exhibited a GQ of <88 and 88, respectively, at 36 months’ chronological age (P = .2). Maternal educational level was low in 73.1% and 83.8% of mothers with infants who exhibited a GQ of <88 and 88, respectively, at 36 months’ chronological age (P = .2). The characteristics of the studied population according to cognitive outcome at 36 months’ age are shown in Table 2.
|
Younger gestational age, being male, ROP of stage 3 or higher, and CLD were associated with a GQ of <88 at 36 months of age. A GQ of <70 was found in 14.2% (n = 20) of children. Abnormal MRI status was found in 72.4% and in 27.6% of infants who exhibited a GQ of <88 and
88, respectively, at 36 months’ chronological age (P < .0001). Mean (SD) weight, length, and HC z scores ranged through the first 36 months of life from –2.62 (1.7) at 3 months to –1.77 (1.3) at 36 months (P < .0001), from –2.67 (1.5) to –1.01 (1.07; P < .0001), and from –1.57 (1.38) to –1.57 (1.03; P = 0.9), respectively. At 36 months, 38%, 17%, and 34% of infants had weight, length, and HC z score less than –2 SD, respectively. Absence of HC catch-up growth at 36 months was associated with a GQ of <88 at 36 months (P < .05).
Neurofunctional Assessment at 12 Months’ Corrected Age and at 36 Months’ Chronological Age
At 12 months’ corrected age, the neurofunctional score was 1 in 82 (58.2%) infants, 2 in 41 (29%), and 3 in 18 (12,8%). The corresponding values at 36 months’ chronological age were 67 (47.5%), 52 (36.9%), and 22 (15.6%) infants. At the age of 36 months, the neurofunctional status improved, unchanged, or deteriorated in 7 (5%), 108 (76.6%), and 26 (18.4%) infants, respectively; 73% and 100% of infants with a score of 1 or 3, respectively, at 12 months’ corrected age had unchanged functional status at 36 months of age. The clinical disabilities of infants who had a neurofunctional score of 2 at 36 months of age were learning disabilities and dyspraxia (23%), clumsiness (23%), behavioral problems (30%), language impairment (10%), psychomotor retardation (12%), and hypoacusia (2%). The clinical features of the infants who had a neurofunctional score of 3 at 36 months of age were cerebral palsy (63%), mental retardation (22%), visual impairment (5%), deafness (5%), and autism spectrum (5%).
Neurofunctional Status at 12 Months’ Corrected Age and Griffiths Mental Development Scale at 36 Months’ Chronological Age
A significant statistical association between the 12-month neurofunctional status and the GQ assessed at 36 months (P < .0001) was found. On posthoc analysis, all comparisons were significant.
Predicting GQ at 36 Months’ Chronological Age From the 12-Month Neurofunctional Assessment
A logistic regression analysis was performed to identify determinants of developmental delay at 36 months (Table 3). For statistical analysis, patients who had a score of 2 at the 12-month neurofunctional evaluation were pooled. Abnormal cranial MRI results at term, CLD, and a score of 1 at the neurofunctional evaluation at 12 months were found to be independently associated with cognitive delay at 36 months.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSAPPENDIX: NEUROFUNCTIONAL...REFERENCES |
|---|
In this study, the 12-month neurofunctional assessment, MRI status at term, and CLD remained predictive of cognitive development at 36 months in ELBW infants, also after adjusting for confounders. In addition, we found that children who were assessed as normal (score
1) at the 12-month neurofunctional assessment showed significantly higher GQ at 36 months of age compared with infants who exhibited dysfunctions (score 2). This finding could be explained by the fact that the detection of dysfunctions at 12 months of age may reflect the difficulty that the infant experiences in the learning process and in the development of new tasks, as a result of impairment of the emerging functions at that age, evaluated by the neurofunctional approach. As a consequence, the normal process of cognition may be impaired. Several authors have found an association between motor function assessed at 12 months and cognitive outcome at school age. Burns et al4 reported that group classification of motor development at age 1 year, investigated using the neurosensory motor developmental assessment, is predictive of cognitive outcome in ELBW infants at age 4 years. Jeyaseelan et al5 reported that motor difficulties, assessed by use of neurosensory motor developmental assessment, in ELBW infants at 2 years are strongly associated with later clinical measures of attention. Roth et al13 and Stewart et al14 found a close relationship between neuromotor impairment, investigated by standardized neurologic examination, and cognitive defects at age 4 years. The results of these studies are consistent with Piaget's theory15 and the mirror neuron system.16, 17 According to Piaget, there is a strict interrelation between motor and cognitive development: action is considered the foundation of knowledge as it is, at first, physical and then it is transformed into mental action and representation. Also, the mirror neuron system, which activates when an individual performs an action, as well as when he or she observes a similar action done by another individual, seems to play an important role in the social cognition process: it seems not only to provide an action recognition mechanism but also to constitute a neural system for coding the intentions of others and allowing imitation learning.18 In addition, according to Hadders-Algra,19 both primary (the phase in which the variation in motor behavior is not geared to external conditions) and secondary (the phase in which the motor performance can be adapted to specific situations) variability and, consequently, the motor repertoire can be reduced in preterm infants as a result of perinatal lesions or abnormal cerebral cortical development. Consistent with these findings, the association of the 12-month neurofunctional evaluation with cognitive performance at 36 months of age may be to some extent explained by the fact that a neurofunctional approach includes the evaluation of evoked and spontaneous motility, postural adaptability, and variability of motor patterns, according to the emerging functions of each age.6 The finding of lower GQ at 36 months in infants who exhibited minor dysfunctions at the 12-month neurofunctional assessment highlights the importance of additional implementation of individualized care plans both during hospital stay and in the postdischarge period because a limited motor repertoire, even in the absence of brain lesions, may result in deficit of processing information and solving problems through the selection of the most appropriate strategies and adaptive solutions. In addition, promoting the infant's neurobehavioral together with motor organization has been reported to be associated with both medical and developmental advantages20; therefore, detection of dysfunctions at the 12-month neurofunctional evaluation may represent an additional clinical tool in identifying infants who are at risk for poor later cognitive outcome and could benefit from early intervention.
Although efforts have been made to eliminate the artificial division between the neurologic and the behavioral approach to the neurodevelopmental assessment of preterm infants, few studies have investigated the relationship between the cognitive outcome of ELBW infants and the neurofunctional evaluation. Wallace et al8 reported that preterm neonates who had poor neurobehavioral performance, assessed as visual-following and auditory-orienting, had significantly lower cognitive test scores at age 1 and 6 years. Costantinou et al7 found that the Neurobehavioral Assessment of the Preterm Infants, evaluated before hospital discharge, correlates with cognitive outcome at 30 months of age.
There is increasing evidence that cognitive domain in preterm infants is one of the most common areas of poor functioning.21 The prevalence of severe developmental delay found in our study is 14.2%. Several multicenter trials2, 22–25 reported different rates of developmental disabilities in very preterm infants, ranging from 15% to 20% up to 35% to 40%. In a meta-analysis, Bhutta et al26 reported that mean cognitive scores of preterm infants at school age were 10.9 lower compared with those of control subjects, showing a linear correlation with birth weight and gestational age. In this study, a younger gestational age, being male, absence of HC catch-up growth at 36 months, and severe ROP were associated with developmental delay at 36 months at univariate analysis. No association with birth weight was found, probably because in our study, infants with birth weight <600 g were unrepresented. Being male, having poor postnatal growth, especially of the head, and having severe ROP have been reported as risk factors for developmental delay by other authors.2, 27, 28
In this study, at logistic regression analysis, also abnormal MRI status at term and the presence of CLD remained predictive of cognitive outcome at 36 months. Abnormal MRI status at term has been reported as a strong predictor of adverse neurodevelopmental outcome by other authors,29 suggesting a role for MRI at term in risk stratification for preterm infants. There is agreement on the unfavorable effect of CLD, even in the absence of severe brain lesions, on cognitive outcome in children who are born very preterm, which seems to persist into school age.30
In our study, maternal education and being SGA were not predictive of later cognitive outcome. The effect of maternal education on cognitive outcome in ELBW infants remains in question. Although several authors have reported lack of maternal education as a risk factor for poor cognitive development,2 others did not observe any effect.4, 5 Current literature is inconclusive also about the role of being SGA in determining neurodevelopment outcome. Some studies31 reported no effect of SGA status on cognitive outcome, whereas others found a modest association between SGA and IQ.32
We did not find any association between sepsis and developmental delay. This finding is in agreement with Vohr et al,2 who did not identify sepsis as predictive of cognitive impairment, whereas Stoll et al33 found a rate of cognitive developmental disability of 33% to 42% in infants with infection versus 22% in infants without infection.
A potential limitation of the findings of this study is the loss to follow-up, which was >10%; however, because the patients who were lost to follow-up had similar characteristics at birth and in the developmental measures, when last assessed, to those reported, this loss is unlikely to bias substantially the associations reported. An additional limitation of this study was that, despite a relatively large sample size, the low rate of severe cognitive impairment precluded a separate analysis to identify the variables that were predictive of a GQ of <70.
Because disability, defined as impairment of function, has been recognized to be multidimensional,34, 35 the choice of outcome classifications and assessments remains difficult. Additional investigations are warranted to identify additional, simple methods of neurodevelopmental assessment in clinical practice that may better reflect the emerging concept of disability and focus the attention on the consequences of disease rather than on disease itself. A functional approach to the neurodevelopmental evaluation that actually investigates not only an infant's motor but also neuromotor and behavioral skills may well relate to later outcomes and focus on the outcome potential of the infant.
|
CONCLUSIONS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSAPPENDIX: NEUROFUNCTIONAL...REFERENCES |
|---|
According to our findings, the presence of a score of
2 at the 12-month neurofunctional assessment represents an early clinical marker of adverse later cognitive outcome. This study suggests that an early neurofunctional evaluation could be an additional useful tool in alerting clinicians to follow up neurodevelopment strictly to initiate early intervention programs. Additional, larger studies are desirable to clarify better the role of the neurofunctional assessment in the early identification of children who are at risk for poor later cognitive performance. |
APPENDIX: NEUROFUNCTIONAL ASSESSMENT OF PREMATURE INFANT AT 12 MONTHS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSAPPENDIX: NEUROFUNCTIONAL...REFERENCES |
|---|
|
|
FOOTNOTES |
|---|
Accepted May 29, 2007.
Address correspondence to Maria Lorella Giannì, MD, Neonatal Intensive Care Unit, Clinica Mangiagalli, IRCS, University Medical School, Via Commenda 12, 20122 Milano, Italy. E-mail: maria.gianni{at}unimi.it
The authors have indicated they have no financial relationships relevant to this article to disclose.
|
REFERENCES |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSAPPENDIX: NEUROFUNCTIONAL...REFERENCES |
|---|
- Draper ES, Manktelow B, Field D, James D. Prediction of survival for preterm births by weight and gestational age: retrospective population based study.
BMJ. 1999;319
:1093
–1097
[Abstract/Free Full Text] - Vohr BR, Wright LL, Dusick AM, et al. Neurodevelopmental and functional outcomes of extremely low birth weight infants in the National Institute of Child Health and Human Development Neonatal Research Network, 1993–1994.
Pediatrics. 2000;105
:1216
–1226
[Abstract/Free Full Text] - Taylor Hg, Klein N, Hack M. School-age consequences of birth weight less than 750 g: a review and an update. Dev Neuropsychol. 2000;17 :289 –321[CrossRef][Web of Science][Medline]
- Burns Y, O'Callaghan M, McDonnel 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[CrossRef][Web of Science][Medline]
- Jeyaseelan D, O'Callaghan M, Neulinger K, Shum D, Burns Y. The association between early minor motor difficulties in extremely low birth weight infants and school age attentional difficulties. Early Hum Dev. 2006;82 :249 –255[CrossRef][Web of Science][Medline]
- Picciolini O, Giannì ML, Vegni C, Fumagalli M, Mosca F. Usefulness of an early neurofunctional assessment in predicting neurodevelopment outcome in very low birth weight infants.
Arch Dis Child Fetal Neonatal Ed. 2006;91
:F111
–F117
[Abstract/Free Full Text] - Costantinou JC, Adamson-Macedo EN, Mirmiran M, Ariagno RL, Fleiser BE. Neurobehavioral assessment predicts differential outcome between VLBW and ELBW preterm infants. J Perinatol. 2005;25 :788 –793[CrossRef][Medline]
- Wallace IF, Rose SA, McCarton CM, Kurtzberg D, Vaughan HG. Relations between infant neurobehavioral performance and cognitive outcome in very low birth weight preterm infants. J Dev Behav Pediatr. 1995;16 :309 –317[Web of Science][Medline]
- Bell MJ, Temberg JL, Feigin RD, et al. Neonatal necrotizing enterocolitis: therapeutic decisions based on clinical staging. Ann Surg. 1978;187 :1 –7[Web of Science][Medline]
- Robertson C. Catch-up growth among very-low-birth-weight preterm infants: a historical perspective. J Pediatr. 2003;143 :145 –146[CrossRef][Web of Science][Medline]
- Agostoni C, Grandi F, Scaglioni S, et al. Growth pattern of breastfed and nonbreastfed infants with atopic dermatitis in the first year of life. Pediatrics. 2000;106(5) . Available at: www.pediatrics.org/cgi/content/full/106/5/e73
- Griffiths R. The Abilities of Young Children: A Comprehensive System of Mental Measurement for the First 8 Years of Life—Child Development Research Centre London. London, England: Young and Son; 1970
- Roth SC, Baudin J, Pezzani-Goldsmith M, Townsend J, Reynolds EO, Stewart AL. Relation between neurodevelopmental status of very preterm infants at one and eight years. Dev Med Child Neurol. 1994;36 :1049 –1062[Web of Science][Medline]
- Stewart AL, de Costello AM, Hamilton PA, et al. Relationship between neurodevelopment status of very preterm infants at one and four years. Dev Med Child Neurol. 1989;31 :756 –765[Web of Science][Medline]
- Piaget J. The Origins of Intelligence in the Child. London, England: Penguin Educational; 1977
- Iacoboni M, Dapretto M. The mirror neuron system and the consequences of its dysfunctions. Nat Rev Neurosci. 2006;7 :942 –951[CrossRef][Web of Science][Medline]
- Rizzolatti G, Craighero L. The mirror neurons system. Annu Rev Neurosci. 2004;27 :169 –192[CrossRef][Web of Science][Medline]
- Iacoboni M, Molnar-Szakacs I. Grasping the intentions of others with one's owns mirror neuron system. PLOS Biol. 2005;3 :529 –535[Web of Science]
- Hadders-Algra M. Early brain damage and the development of motor behavior in children: clues for therapeutic intervention? Neural Plast. 2001;8 :31 –49[Medline]
- Als H, Lawhon G, Brown E, et al. Individualized behavioural and environmental care for the very low birth weight preterm infant at high risk for bronchopulmonary dysplasia: neonatal intensive care unit and developmental outcome.
Pediatrics. 1986;78
:1123
–1132
[Abstract/Free Full Text] - Marlow N. Introduction: neurodevelopmental follow-up after preterm birth. Early Hum Dev. 2006;82 :149 –150[CrossRef][Web of Science]
- Finnstrom O, Otterblad O, Sedin G, et al. Neurosensory outcome and growth at three years in extremely low birth weight infants: follow-up results from the Swedish national prospective study. Acta Paediatr. 1998;87 :1055 –1060[CrossRef][Web of Science][Medline]
- Doyle LW; Victorian Infant Collaborative Study Group. Outcome at 5 years of age of children 23 to 27 weeks’ gestation: refining the prognosis.
Pediatrics. 2001;108
:134
–141
[Abstract/Free Full Text] - Wood NS, Marlow N, Costeloe K, Gibson AT, Wilkinson AR. Neurologic and developmental disability after extreme preterm birth.
N Engl J Med. 2000;343
:378
–384
[Abstract/Free Full Text] - Schmidt B, Asztalos EV, Roberts RS, et al. Impact of bronchopulmonary dysplasia, brain injury, and severe retinopathy on the outcome of the extremely low birth weight infants at 18 months: results from the trail of indomethacin prophylaxis in preterms.
JAMA. 2003;289
:1124
–1129
[Abstract/Free Full Text] - Bhutta AT, Cleves AM, Casey PH, Cradock MM, Anand KJ. Cognitive and behavioural outcomes of school-aged children who were born preterm.
JAMA. 2002;288
:728
–737
[Abstract/Free Full Text] - Msall ME, Phelps DL, DiGaudio KM, et al. Severity of neonatal retinopathy of prematurity is predictive of neurodevelopmental functional outcome at age 5.5 years.
Pediatrics. 2000;106
:998
–1005
[Abstract/Free Full Text] - Latal-Hajnal LH, von Siebenthal K, Kovari H, Bucher HU, Largo RH. Postnatal growth in VLBW infants: significant association with neurodevelopmental outcome. J Pediatr. 2003;143 :163 –170[Web of Science][Medline]
- Woodward LJ, Anderson PJ, Austin NC, Howard K, Inder TE. Neonatal MRI to predict neurodevelopmental outcomes in preterm infants.
N Engl J Med. 2006;355
:685
–694
[Abstract/Free Full Text] - Böhm B, Katz-Salamon M. Cognitive development at 5.5 years of children with chronic lung disease of prematurity.
Arch Dis Child Fetal Neonatal Ed. 2003;88
:F101
–F105
[Abstract/Free Full Text] - Martyn CN, Gale CR, Sayer AA, Fall C. Growth in utero and cognitive function in adult life: follow up study of people born between 1920 and 1943.
BMJ. 1996;312
:1393
–1396
[Abstract/Free Full Text] - Hollo O, Rautava P, Korhonen T, Helenius H, Kero P, Sillanpaa M. Academic achievement of small-for-gestational age children at age 10 years.
Arch Pediatr Adolesc Med. 2002;156
:179
–187
[Abstract/Free Full Text] - Stoll BJ, Hansen NI, Adams-Chapman I, et al. Neurodevelopmental and growth impairment among extremely low birth weight infants with neonatal infection.
JAMA. 2004;292
:2357
–2365
[Abstract/Free Full Text] - Msall ME. Neurodevelopmental surveillance in the first 2 years after extremely preterm birth: evidence, challenges, and guidelines. Early Hum Dev. 2006;82 :157 –166[CrossRef][Web of Science][Medline]
- World Health Organization. International Classification of Functioning, Disability and Health. Geneva, Switzerland: World Health Organization; 2001
PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics
CiteULike 
Connotea 
Del.icio.us 
Digg 
Facebook 
Reddit 
Technorati 
Twitter What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
