Skip Navigation


American Journal of Epidemiology Advance Access originally published online on September 26, 2007
American Journal of Epidemiology 2008 167(1):103-111; doi:10.1093/aje/kwm245
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
167/1/103    most recent
kwm245v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (3)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Leonard, H.
Right arrow Articles by Bower, C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Leonard, H.
Right arrow Articles by Bower, C.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

American Journal of Epidemiology © The Author 2007. Published by the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

ORIGINAL CONTRIBUTIONS

Relation between Intrauterine Growth and Subsequent Intellectual Disability in a Ten-year Population Cohort of Children in Western Australia

Helen Leonard1, Natasha Nassar1, Jenny Bourke1, Eve Blair1, Seonaid Mulroy2, Nicholas de Klerk1 and Carol Bower1,3

1 Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, West Perth, Australia
2 King Edward Memorial Hospital for Women, Subiaco, Australia
3 Birth Defects Registry, Women and Children's Health Service, Perth, Australia

Correspondence to Dr. Helen Leonard, Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, P.O. Box 855, West Perth 6872, Western Australia, Australia (e-mail: hleonard{at}ichr.uwa.edu.au).

Received for publication February 7, 2007. Accepted for publication August 1, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The authors investigated the association between intrauterine growth and intellectual disability (ID). The appropriateness of intrauterine growth was assessed using percentage of optimal birth weight, a measure that accounts for gestational age, maternal height, parity, and infant sex. Using population-based record linkage, singleton Caucasian and Aboriginal children born in Western Australia in 1983–1992 and alive in 2002 with ID of unknown cause (n = 2,625) were compared with children without ID (n = 217,252). The odds of ID increased with less-than-optimal intrauterine growth. In Caucasian children, after adjustment for sociodemographic factors, severe growth restriction was associated with development of mild–moderate ID among preterm births (<37 weeks) (odds ratio (OR) = 1.71, 95% confidence interval (CI): 1.06, 2.77) and term births (≥37 weeks) (OR = 2.42, 95% CI: 1.88, 3.12) and with severe ID (OR = 4.79, 95% CI: 2.59, 8.83) among term births. Effects were similar among Aboriginal children. Severe growth restriction (OR = 3.2, 95% CI: 1.3, 7.9) and poor head growth (OR = 3.6, 95% CI: 1.4, 9.0) were independently associated with severe ID. Infants with excess intrauterine growth were more likely to be diagnosed with ID associated with autism spectrum disorder (OR = 2.36, 95% CI: 0.93, 6.03). These findings suggest that inappropriate intrauterine growth, less than or greater than optimal birth weight, is associated with development of ID.

Australia; cohort studies; developmental disabilities; fetal development; fetal growth retardation; medical record linkage; mental retardation; pediatrics

Abbreviations: CI, confidence interval; POBW, percentage of optimal birth weight


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The adverse sequelae of both prematurity and low birth weight in terms of neonatal survival and major morbidity are well recognized and have long been studied. In recent decades, there has been a marked improvement in the survival of extremely low birth weight infants, and this has resulted in growing concern regarding their long-term neurologic outcomes, including the possibility of intellectual disability (1).

A systematic review of 15 studies and meta-analysis by Bhutta et al. (2) found that preterm birth was associated with lower cognitive score and that intelligence quotient was directly correlated with the degree of prematurity. However, a systematic review does not overcome the potential biases that may exist in individual studies, especially if the biases tend to point in the same direction for all studies. Many of the studies that have investigated cognitive outcomes in very preterm or extremely low birth weight children have involved relatively small numbers or have been based on cases from a single center (1, 3–9). There has also been concern that the children and families accessible for follow-up may differ systematically from those who cannot be followed (10–12).

Low birth weight is often used as an indicator of intrauterine growth and has been associated with adverse neurologic outcomes, including speech and language problems, cognitive and behavioral problems, and educational, learning, developmental, and intellectual disabilities (4–8, 13, 14). Several population-based studies have been undertaken, but often they have been restricted to children in a specific gestational-age category or birth weight group (15). In addition, a number of factors that are likely to influence infant outcomes, such as race (16–19), gender (16, 17), and socioeconomic status (18, 19), have often not been taken into account. In some of these studies, investigators have taken a population-based approach to the investigation of low birth weight but have based their outcomes only on the need for special education (18, 20–22). In other studies, investigators have taken the reverse approach, studying cohorts of children with intellectual disability and inferring etiology from retrospectively collected antenatal and perinatal information (23, 24).

The risk of poor outcomes for an infant is dependent on both the duration of gestation and the appropriateness of intrauterine growth. Intrauterine growth restriction infers that some suboptimal genetic and/or environmental factor has restricted fetal growth (25). At some point in gestation, the growth trajectory has deviated negatively from that expected for the growth-determining characteristics of that fetus, and consequently the neonate is smaller than anticipated given those inherent characteristics. Intrauterine growth is often inferred from size at birth, taking duration of gestation into account. Thus, being born small for gestational age is often taken as a surrogate for intrauterine growth restriction. Since not all neonates ought to be the same size, the assessment of the appropriateness of intrauterine growth from birth size should also take nonpathologic determinants of size into account (26). Inadequate head growth has also been associated with poor developmental outcomes (3, 27, 28), with Strauss et al. (29) showing that microcephaly in a poorly grown infant increases the likelihood of an adverse effect on neurodevelopment.

In this study, a Western Australian population-based record linkage study, we assessed the association between the appropriateness of intrauterine growth and the development of intellectual disability in children.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
A population-based cohort study was undertaken in which all children born in Western Australia between 1983 and 1992 and alive in 2002 (n = 240,351) who were identified as having an intellectual disability of unknown cause were compared with children without intellectual disability. Record linkage was used to combine Western Australian population data on children with intellectual disability with birth data from the Midwives' Notification System, a statutory collection of antenatal and perinatal details on every birth attended by a midwife (99.5 percent of births) in Western Australia (30). The two sources of ascertainment for what is now known as the IDEA (Intellectual Disability Exploring Answers) Database (31) are 1) registrations from the Disability Services Commission, the main provider of services for children and adults with intellectual disability in Western Australia, and 2) the government and nongovernment agencies providing educational services to children with intellectual disability in Western Australia. Children from these sources are eligible to be included in the IDEA Database if they have an intelligence quotient less than 70 or a medical condition unequivocally accepted as being associated with intellectual disability. Children registered with the Disability Services Commission generally either have been clinically assessed or have had clinical information extracted by medical staff to identify any recognized etiology for their intellectual disability.

Overall, there were 3,387 children born in Western Australia between 1983 and 1992 who were identified by 1999 as having an intellectual disability, whose births linked to their midwife-completed birth records, and who were alive in 2002. As previously defined (32), 522 of the 3,387 children (15.4 percent) had been assigned a clear medical cause for their intellectual disability (e.g., chromosomal anomalies, Mendelian conditions, or postnatal injury), and these cases were excluded from this analysis. The remaining 2,865 cases of intellectual disability without a known cause were categorized into groups of children with mild-to-moderate intellectual disability (n = 2,462; 85.9 percent), severe or profound intellectual disability (n = 212; 7.4 percent), or intellectual disability associated with autism spectrum disorder (n = 191; 6.7 percent). Cases of mild and moderate intellectual disability identified from education services were already grouped together, and hence, we also grouped cases from the Disability Services Commission in the same way to ensure comparability between the two data sources. The diagnosis of autism spectrum disorder in Western Australia during the study period was made according to the recommendations of the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (33). There were 361 children in whom the level of intellectual disability was unspecified, and these children were included in the mild–moderate group, as it was unlikely that cases of severe intellectual disability would be missed and not registered with the Disability Services Commission (34).

Birth weight (<1,000, 1,000–1,499, 1,500–1,999, 2,000–2,499, 2,500–2,999, 3,000–3,499, 3,500–3,999, 4,000–4,499, or >4,500 g) and gestational age (<33, 33–36, or ≥37 weeks, with preterm being defined as <37 weeks' gestation) were categorized as given. Appropriateness of intrauterine growth was assessed using percentage of optimal birth weight (POBW). The optimal birth weight for a neonate was first determined by applying the model developed in a previous study, which was based on data from the 1998–2002 Western Australian birth cohort (26). Only cases without known risk factors for intrauterine growth anomaly (including maternal smoking, vascular disease, preexisting or gestational diabetes, TORCH (toxoplasma, other, rubella, cytomegalovirus, herpes) infections, or birth defects) were included, while taking into account gestational age, infant sex, maternal height, and parity (26). (For a given set of nonpathologic conditions, the estimated optimal birth weight is therefore higher than the population mean birth weight, particularly for preterm births.) POBW was then calculated on the basis of the ratio of observed birth weight to optimal birth weight, and the percentage was categorized into seven groups—<75, 75–<85, 85–<95, 95–<105, 105–<115, 115–<125, and ≥125 percent—with the middle group, 95–<105 percent, being used as the referent in the analysis. The reference group comprised 32.1 percent of the total population; POBW <85 percent was equivalent to approximately less than the 10th percentile of optimal birth weight (26), and POBW >115 percent was equivalent to greater than the 90th percentile of optimal birth weight. Percentage of optimal birth head circumference, a measure of the appropriateness of head growth, was also examined. Information on birth head circumference was available only for the years 1990–1992, reducing the sample size for this analysis to 70,336. The joint and separate effects of severe intrauterine growth restriction and poor head growth were evaluated for Caucasian children by dichotomizing percentage of optimal birth head circumference and POBW based on the cutoff value of each measure being set at two standard deviations below the mean, which gives a value of <92.3 percent for percentage of optimal birth head circumference and <77.1 percent for POBW. Population attributable risks were calculated to examine the proportions of severe intellectual disability and mild–moderate intellectual disability that could be attributed to severe growth restriction in isolation, poor head growth in isolation, and severe growth restriction combined with poor head growth.

On the basis of previous analyses (32), we adjusted for the following sociodemographic variables: marital status, maternal country of birth, health insurance status, paternal occupation, geographic remoteness, and socioeconomic well-being. The last measure was one of the Socio-Economic Indexes for Areas (35) and incorporated the mean ranking of "education and occupation" at the level of the census collection district (comprising about 200 dwellings). We adjusted for geographic remoteness from major service centers using the Accessibility/Remoteness Index of Australia (36). We also adjusted for birth year to take into account secular trends that may have occurred during the study period.

The association between appropriateness of intrauterine growth and intellectual disability was investigated by comparing POBW among children in each category of intellectual disability with children without intellectual disability. The analysis was limited to singleton survivors in 2002 and carried out separately for the children of Caucasian and Aboriginal mothers, since previous studies have shown intellectual disability to be independently associated with maternal ethnicity (32). Thus, we excluded multiple births, children with a medical cause of intellectual disability, and infants born to mothers from non-Caucasian or non-Aboriginal backgrounds (n = 20,474). This resulted in a sample of 219,877 births (2,625 children with intellectual disability of unknown cause and 217,252 children without intellectual disability). We also conducted an analysis stratified by infant sex and preterm birth status (preterm birth (<37 completed weeks' gestation) vs. term birth (≥37 completed weeks)). Descriptive and logistic regression analyses were carried out using Stata, version 9 (37). We also conducted multivariable analysis to adjust for potentially confounding effects of socioeconomic variables and birth year. The results are presented as odds ratios with 95 percent confidence intervals and were considered statistically significant at a level of p < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Among Western Australian singleton children born in 1983–1992 and alive in 2002, a total of 2,277 Caucasian children and 348 Aboriginal children were diagnosed with an intellectual disability of unknown cause, including intellectual disability associated with autism spectrum disorder. For children from Caucasian backgrounds, the odds of mild–moderate intellectual disability increased with decreasing birth weight, reaching 8.9 (95 percent confidence interval (CI): 5.4, 14.6) for birth weight <1,000 g, and with decreasing gestational age, reaching 3.4 (95 percent CI: 2.5, 4.6) at <33 weeks' gestation (table 1). Very few children with severe intellectual disability were born below 1,500 g or before 33 weeks' gestation, but otherwise the trends were similar (table 1). Similar results were found for Aboriginal children, but the numbers of children with severe intellectual disability were small. There were no associations between birth weight or gestational age and the odds of autism spectrum disorder (table 1).


View this table:
[in this window]
[in a new window]

  		TABLE 1. Crude odds ratios for intellectual disability in Caucasian and Aboriginal children born in Western Australia in 1983–1992 and alive in 2002, by birth weight and gestational age

 
The trends in the relation between POBW and intellectual disability were similar to those for birth weight and gestational age and are presented in table 2. Subsequent adjustment for sociodemographic variables and birth year slightly attenuated the odds of intellectual disability among Caucasian children, and the odds ratio for autism spectrum disorder was no longer statistically significant (table 2). Compared with optimal birth weight (POBW 95–<105 percent), the odds ratio for mild–moderate intellectual disability in Caucasian infants increased with decreasing POBW, to 2.42 (95 percent CI: 1.93, 3.05) for infants with severe growth restriction (POBW <75 percent). Poor fetal growth (POBW <75 percent) was associated with a greater than threefold increase in severe intellectual disability (odds ratio = 3.64, 95 percent CI: 2.00, 6.64). Infants with excess intrauterine growth (POBW >124 percent) were more likely to be diagnosed with intellectual disability associated with autism spectrum disorder, but the confidence interval around the estimate was wide (odds ratio = 2.36, 95 percent CI: 0.93, 6.03) (table 2). The effect of poor intrauterine growth among Aboriginal children was smaller for mild–moderate intellectual disability but larger for severe intellectual disability; however, statistical significance could not be expected with such small numbers (table 2).


View this table:
[in this window]
[in a new window]

  		TABLE 2. Crude and adjusted* odds ratios for intellectual disability in Caucasian and Aboriginal children born in Western Australia in 1983–1992 and alive in 2002, by percentage of optimal birth weight

 
Analysis by infant sex revealed no differences between males and females (table 3). Stratification by preterm birth status showed that the association between POBW and intellectual disability was greater among term infants (table 3). Less-than-optimal fetal growth (POBW <85 percent) was associated with mild–moderate intellectual disability in both preterm and term infants, whereas for severe intellectual disability, the association was found exclusively among term infants with severe growth restriction (POBW <75 percent) (table 3).


View this table:
[in this window]
[in a new window]

  		TABLE 3. Adjusted* odds ratios for intellectual disability according to percentage of optimal birth weight in Caucasian and Aboriginal children born in Western Australia in 1983–1992 and alive in 2002, by infant sex and preterm birth status

 
Severe growth restriction (POBW <77.1 percent) and poor head growth (percentage of optimal birth head circumference <92.3 percent) were independently associated with increased odds of both mild–moderate and severe intellectual disability (table 4). In the bivariate analysis for mild–moderate intellectual disability, the statistically significant association with severe growth restriction in isolation remained, but that with poor head growth was no longer statistically significant. The odds ratio for their interaction variable was positive but did not reach statistical significance (table 4). In bivariate analysis for severe intellectual disability, the pattern of association was different in that the associations with poor head growth and severe growth restriction both remained statistically significant; each had an estimate of attributable risk of almost 6 percent. Their interaction variable was not associated with severe intellectual disability (table 4).


View this table:
[in this window]
[in a new window]

  		TABLE 4. Association of severe growth restriction (percentage of optimal birth weight <77.1%) and poor head growth (percentage of optimal birth head circumference <92.3%) with intellectual disability among Caucasian children born in Western Australia in 1990–1992 and alive in 2002

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Our results highlight that inappropriate intrauterine growth is associated with development of intellectual disability among children. After adjustment for sociodemographic factors, less-than-optimal intrauterine growth among Caucasian children was associated with mild–moderate intellectual disability, irrespective of gestational age. Severe growth restriction was associated with severe intellectual disability, although the effect was found predominantly among term births. The effects were also similar among Aboriginal children. Severe growth restriction and poor head growth were independently associated with severe intellectual disability, while infants with excess intrauterine growth were more likely to be diagnosed with intellectual disability associated with autism spectrum disorder.

One strength of this study is that it was able to identify and analyze intellectual disability diagnosed up to 1999 in 2,277 children born from 1983 to 1992. Many other studies have had more limited follow-up and have struggled to achieve an adequate sample size (12). Use of record linkage to combine data from several existing sources, including the state agency providing medical services (the Disability Services Commission) and three agencies providing educational services, all of which have similar assessment criteria, also increased case ascertainment. We considered a 10-year birth cohort selected from the total population of Western Australia (approximately 1.8 million) to provide a reasonable sample of survivors in each POBW category, particularly for Caucasian children. Since we used the entire population of Western Australia as our comparison group, we also avoided possible bias in the selection of controls (38), and information collected at birth is not subject to recall bias. The geography of Western Australia also ensured a relatively stable population, with little of the geographic mobility encountered in other studies (38). As a result, our population-based data linkage study was less affected by loss to follow-up, which is often associated with social disadvantage, itself a risk factor for adverse outcomes. However, while our study has been able to follow children well into school age, it is still too early to compare the study cohort outcomes with those of a more recently born cohort.

The restandardization of tests and the revision of criteria for intellectual disability is an ongoing problem for the evaluation of longitudinal data and secular trends (39). In this study, we attempted to take such reclassification into account and to be consistent in our classification of intellectual disability over time (31). However, one of the limitations of our study is that we could not estimate the more subtle effects of intrauterine growth on mild learning disabilities and behavior problems, since population-based data on behavioral outcomes such as attention deficit hyperactivity disorder do not exist. However, it is our belief that intellectual disability can be considered a barometer for these more subtle effects. It is also likely that the older children in our cohort were more likely to have obtained a diagnosis of intellectual disability or autism spectrum disorder, as they would have been at school longer and had a greater window for identification than the younger children. Since this study was based on children who survived to 2002, the number of cases of severe intellectual disability may have been underestimated due to increased early mortality among these children. We also acknowledge that intellectual disability is heterogeneous with respect to etiology, and it is likely that intrauterine growth takes different roles in different causal pathways. However, since these cases were selected on the basis of unknown etiology, this could not be investigated.

Birth weight is a function of both the appropriateness of intrauterine growth and length of gestation. However, in an examination of the effects of low birth weight alone, it is not possible to distinguish the effects of short gestation from those of poor intrauterine growth. There have only been a few studies examining the impact of poor intrauterine growth, rather than prematurity or low birth weight per se, on cognitive outcome. In a recent review, Pallotto and Kilbride (40) identified follow-up studies of term small-for-gestational-age infants and compared their developmental outcomes with those of children of appropriate size for gestational age. The studies reviewed used different outcome measures, and several related to children born in the 1960s or 1970s, but most showed a modest effect of smallness for gestational age on intelligence quotient. Another review by Yanney and Marlow (27) also highlighted the association of fetal growth restriction with neurodevelopmental disability, including cerebral palsy, cognitive deficit, and behavioral problems. In a recent review of high-quality population-based studies, only two studies had investigated the relation between smallness for gestational age and autism spectrum disorder, and both found an increased risk (41).

POBW measures appropriateness of growth by comparing birth weight with that observed for infants of the same sex, gestation, and maternal height in a population of births not exposed to any of the common factors restricting growth. It is on account of this last factor that the measure lays claim to being the percentage of optimal growth, rather than that of the mean, median, expected, or observed growth. It is therefore independent of the proportion of pregnancies affected by growth-restricting conditions in the population under study. It has frequently been observed that preterm infants are much more likely to be growth-restricted than infants who are born at term, and on this account growth standards based on birth weights of preterm infants underestimate the extent to which they are growth-restricted. A recent study by Zubrick et al. (42) was one of the first to use POBW as a measure of intrauterine growth. Zubrick et al. reported that children below the second percentile were at significantly increased risk of mental health morbidity and were more likely to be rated as academically impaired (42). Similar methods and results were also found in a study investigating the relation between cerebral palsy and intrauterine growth (43). In that study, weight-for-gestational-age z scores were calculated using sex-specific fetal growth curves. The z scores showed that abnormal intrauterine growth, both small and large, was associated with a more severe form of cerebral palsy (43). Given the increased tendency toward poorer developmental outcomes among children born smaller or larger than optimal birth weight, further research to investigate the etiology of abnormal fetal growth is important. In particular, the role of maternal diabetes, which can result in under- or overgrowth of the fetus, will be an important factor to examine, as it has already been shown to be associated with increased risk of mild–moderate intellectual disability and autism spectrum disorder associated with intellectual disability (44).

In our study, the joint analysis of severe growth restriction and poor head growth shows an interesting difference between our two categories of intellectual disability. Severe intellectual disability was strongly and independently associated with both poor head growth and severe growth restriction, and both factors independently contributed equally (6 percent) to the development of severe intellectual disability. This suggests two independent etiologic pathways, one operating primarily via poor head growth without severe growth restriction and one operating primarily via severe growth restriction without poor head growth, which is suggestive of later-onset growth restriction. However, given the small number of children with severe intellectual disability in our sample, care must be taken to not overinterpret these results until larger studies can confirm the findings. In contrast, for mild–moderate intellectual disability, the association was entirely due to severe growth restriction associated with poor head growth, which is suggestive of very-early-onset growth restriction. The effect of genetic or environmental factors, such as chromosomal abnormalities or intrauterine infections, on the outcome in pathologic or symmetric growth restriction is also clearly an issue (27, 40, 45). In this study, it was our intention to exclude all children with known biomedical causes of intellectual disability from the case group. However, it is possible that some undiagnosed cases could still have inadvertently been included. A number of authors have highlighted the need for further research when investigating the effect of head growth on neurodevelopmental outcomes associated with growth restriction, especially in view of the multiple interrelated factors that affect neurodevelopment both antenatally and postnatally (27, 40, 45).

To our knowledge, this was the first study to investigate intrauterine growth and intellectual disability using POBW, an appropriate measure of fetal growth. For both Caucasian and Aboriginal children, the most vulnerable infants born with severe growth restriction, particularly at term, had the greatest odds of developing intellectual disability, and there was a consistent association between excess intrauterine growth and intellectual disability associated with autism spectrum disorder. These results suggest that the underlying etiology of inappropriate intrauterine growth and its association with intellectual disability varies with the type and severity of the developmental outcome, and further investigation is required to determine whether inappropriate growth is a predictor or cause of intellectual disability. These findings provide important information for clinicians and parents in the follow-up, screening, and management of infants most at risk of intellectual disability and the possibility of early intervention for reducing poor developmental outcomes in the future.


   ACKNOWLEDGMENTS
 
This study was supported by Program Grant 353514 from the Australian National Health and Medical Research Council (NHMRC), NHMRC Research Fellowship 353628 (Dr. Bower), and NHMRC Public Health (Australia) Fellowship 404118 (Dr. Nassar).

The authors are grateful to the Disability Services Commission, the Telethon Institute for Child Health Research, the Western Australia Department of Education and Training, the Catholic Education Office, the Association of Independent Schools of Western Australia, and the Birth Defects Registry for assistance with data collection and other aspects of the study, including organizational support. They particularly thank Harry Bouckley, Elvira Edwards, Jane Pavledis, Mairead McCoy, Tessa Vincent, Maureen Thomson, Audrey Jackson, Peter Cosgrove, and Huan Ngyuen.

The study protocol was approved by the ethics committee of the Women's and Children's Health Service (673/EP), the University of Western Australia (05/06/004/K66), and the Confidentiality of Health Information Committee of the Department of Health (97015), Western Australia.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Wilson-Costello D, Friedman H, Minich N, et al. Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics (2005) 115:997–1003.[Abstract/Free Full Text]
  2. Bhutta AT, Cleves MA, Casey PH, et al. Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA (2002) 288:728–37.[Abstract/Free Full Text]
  3. Cooke RW. Perinatal and postnatal factors in very preterm infants and subsequent cognitive and motor abilities. Arch Dis Child Fetal Neonatal Ed (2005) 90:F60–3.[Abstract/Free Full Text]
  4. Puga B, Ferrandez Longas A, Garcia Romero R, et al. Psychomotor and intellectual development of children born with intrauterine growth retardation (IUGR). J Pediatr Endocrinol Metab (2004) 17(suppl 3):457–62.[Web of Science]
  5. Kok JH, den Ouden AL, Verloove-Vanhorick SP, et al. Outcome of very preterm small for gestational age infants: the first nine years of life. Br J Obstet Gynaecol (1998) 105:162–8.[Web of Science][Medline]
  6. Kato EH, Yamada H, Matsumoto Y, et al. Relation between perinatal factors and outcome of very low birth weight infants. J Perinat Med (1996) 24:677–86.[Web of Science][Medline]
  7. Halsey CL, Collin MF, Anderson CL. Extremely low-birth-weight children and their peers. A comparison of school-age outcomes. Arch Pediatr Adolesc Med (1996) 150:790–4.[Abstract/Free Full Text]
  8. Whitfield MF, Grunau RV, Holsti L. Extremely premature (< or = 800 g) schoolchildren: multiple areas of hidden disability. Arch Dis Child Fetal Neonatal Ed (1997) 77:F85–90.[Abstract/Free Full Text]
  9. Hack M, Taylor HG, Drotar D, et al. Chronic conditions, functional limitations, and special health care needs of school-aged children born with extremely low-birth-weight in the 1990s. JAMA (2005) 294:318–25.[Abstract/Free Full Text]
  10. Tin W, Fritz S, Wariyar U, et al. Outcome of very preterm birth: children reviewed with ease at 2 years differ from those followed up with difficulty. Arch Dis Child Fetal Neonatal Ed (1998) 79:F83–7.[Abstract/Free Full Text]
  11. Callanan C, Doyle L, Rickards A, et al. Children followed with difficulty: how do they differ? J Paediatr Child Health (2001) 37:152–6.[CrossRef][Web of Science][Medline]
  12. Tyson JE, Saigal S. Outcomes for extremely low-birth-weight infants: disappointing news. JAMA (2005) 294:371–3.[Free Full Text]
  13. Hack M, Breslau N, Weissman B, et al. Effect of very low birth weight and subnormal head size on cognitive abilities at school age. N Engl J Med (1991) 325:231–7.[Abstract]
  14. Hack M, Klein NK, Taylor HG. Long-term developmental outcomes of low birth weight infants. Future Child (1995) 5:176–96.[CrossRef][Web of Science][Medline]
  15. Stjernqvist K, Svenningsen N. Ten-year follow-up of children born before 29 gestational weeks: health, cognitive development, behaviour and school achievement. Acta Paediatr (1999) 88:557–62.[CrossRef][Web of Science][Medline]
  16. Gissler M, Jarvelin MR, Louhiala P, et al. Boys have more health problems in childhood than girls: follow-up of the 1987 Finnish birth cohort. Acta Paediatr (1999) 88:310–14.[CrossRef][Web of Science][Medline]
  17. Stevenson DK, Verter J, Fanaroff AA, et al. Sex differences in outcomes of very low birthweight infants: the newborn male disadvantage. Arch Dis Child Fetal Neonatal Ed (2000) 83:F182–5.[Abstract/Free Full Text]
  18. Blair C, Scott KG. Proportion of LD placements associated with low socioeconomic status: evidence for a gradient? J Spec Educ (2002) 36:14–22.
  19. Sundrum R, Logan S, Wallace A, et al. Cerebral palsy and socioeconomic status: a retrospective cohort study. Arch Dis Child (2005) 90:15–18.[Abstract/Free Full Text]
  20. Hollomon HA, Scott KG. Influence of birth weight on educational outcomes at age 9: the Miami site of the Infant Health and Development Program. J Dev Behav Pediatr (1998) 19:404–10.[Web of Science][Medline]
  21. Resnick MB, Gueorguieva RV, Carter RL, et al. The impact of low birth weight, perinatal conditions, and sociodemographic factors on educational outcome in kindergarten. Pediatrics (1999) 104:e74. (Electronic article).[Abstract/Free Full Text]
  22. Avchen RN, Scott KG, Mason CA. Birth weight and school-age disabilities: a population-based study. Am J Epidemiol (2001) 154:895–901.[Abstract/Free Full Text]
  23. Blomquist HK, Gustavson KH, Holmgren G. Mild mental retardation in children in a northern Swedish county. J Ment Defic Res (1981) 25:169–86.[Web of Science][Medline]
  24. Gustavson KH, Hagberg B, Hagberg G, et al. Severe mental retardation in a Swedish county. I. Epidemiology, gestational age, birth weight and associated CNS handicaps in children born 1959 –70. Acta Paediatr Scand (1977) 66:373–9.[Web of Science][Medline]
  25. Baker P, Kingdom J, Blair E. Definitions of IUGR. In: Intrauterine growth restriction: aetiology and management—Kingdom J, Baker P, eds. (2000) New York, NY: Springer-Verlag Publishers. 1–4.
  26. Blair EM, Liu Y, de Klerk NH, et al. Optimal fetal growth for the Caucasian singleton and assessment of appropriateness of fetal growth: an analysis of a total population perinatal database. BMC Pediatr (2005) 5:13. (Electronic article).[CrossRef][Medline]
  27. Yanney M, Marlow N. Paediatric consequences of fetal growth restriction. Semin Fetal Neonatal Med (2004) 9:411–18.[CrossRef][Medline]
  28. Bucher HU, Killer C, Ochsner Y, et al. Growth, developmental milestones and health problems in the first 2 years in very preterm infants compared with term infants: a population based study. Eur J Pediatr (2002) 161:151–6.[CrossRef][Web of Science][Medline]
  29. Strauss RS, Dietz WH. Growth and development of term children born with low birth weight: effects of genetic and environmental factors. J Pediatr (1998) 133:67–72.[CrossRef][Web of Science][Medline]
  30. Gee V. Perinatal statistics in Western Australia: annual report of the Western Australian Midwives Notification System 1988. Perth, (1990) Australia: Health Department of Western Australia.
  31. Petterson B, Leonard H, Bourke J, et al. IDEA (Intellectual Disability Exploring Answers): a population based database for intellectual disability in Western Australia. Ann Hum Biol (2005) 32:237–43.[CrossRef][Web of Science][Medline]
  32. Leonard H, Petterson B, De Klerk N, et al. Association of sociodemographic characteristics of children with intellectual disability in Western Australia. Soc Sci Med (2005) 60:1499–513.[CrossRef][Web of Science][Medline]
  33. American Psychiatric Association. Diagnostic and statistical manual of mental disorders, fourth edition (DSM-IV). (1994) Washington, DC: American Psychiatric Association.
  34. Leonard H, Petterson B, Bower C, et al. Prevalence of intellectual disability in Western Australia. Paediatr Perinat Epidemiol (2003) 17:58–67.[CrossRef][Web of Science][Medline]
  35. Australian Bureau of Statistics. Information paper: 1996 Census Socio-Economic Indexes for Areas (SEIFA). (ABS catalogue no. 2039.0). Canberra, (1998) Australia: Australian Bureau of Statistics.
  36. Commonwealth Department of Health and Aged Care. Measuring remoteness: Accessibility/Remoteness Index of Australia (ARIA). Revised edition. (Occasional Papers: New Series no. 14). Canberra, (2001) Australia: Commonwealth Department of Health and Aged Care.
  37. Stata Corporation. Stata statistical software, version 9.0. (2005) College Station, TX: Stata Corporation.
  38. Saigal S. Follow-up of very low birthweight babies to adolescence. Semin Neonatol (2000) 5:107–18.[CrossRef][Medline]
  39. Leonard H, Wen XY. The epidemiology of mental retardation: challenges and opportunities in the new millennium. Ment Retard Dev Disabil Res Rev (2002) 8:117–34.[CrossRef][Web of Science][Medline]
  40. Pallotto EK, Kilbride HW. Perinatal outcome and later implications of intrauterine growth restriction. Clin Obstet Gynecol (2006) 49:257–69.[CrossRef][Web of Science][Medline]
  41. Kolevzon A, Gross R, Reichenberg A. Prenatal and perinatal risk factors for autism: a review and integration of findings. Arch Pediatr Adolesc Med (2007) 161:326–33.[Abstract/Free Full Text]
  42. Zubrick SR, Kurinczuk JJ, McDermott BM, et al. Fetal growth and subsequent mental health problems in children aged 4 to 13 years. Dev Med Child Neurol (2000) 42:14–20.[CrossRef][Web of Science][Medline]
  43. Jarvis S, Glinianaia SV, Arnaud C, et al. Case gender and severity in cerebral palsy varies with intrauterine growth. Arch Dis Child (2005) 90:474–9.[Abstract/Free Full Text]
  44. Leonard H, de Klerk N, Bourke J, et al. Maternal health in pregnancy and intellectual disability in the offspring: a population-based study. Ann Epidemiol (2006) 16:448–54.[CrossRef][Web of Science][Medline]
  45. Georgieff MK. Intrauterine growth retardation and subsequent somatic growth and neurodevelopment. J Pediatr (1998) 133:3–5.[CrossRef][Web of Science][Medline]

Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Am J EpidemiolHome page
O. S. von Ehrenstein, R. T. Mikolajczyk, and J. Zhang
Timing and Trajectories of Fetal Growth Related to Cognitive Development in Childhood
Am. J. Epidemiol., December 1, 2009; 170(11): 1388 - 1395.
[Abstract] [Full Text] [PDF]

Home page
 PediatricsHome page
S. Buchmayer, S. Johansson, A. Johansson, C. M. Hultman, P. Sparen, and S. Cnattingius
Can Association Between Preterm Birth and Autism be Explained by Maternal or Neonatal Morbidity?
Pediatrics, November 1, 2009; 124(5): e817 - e825.
[Abstract] [Full Text] [PDF]

Home page
 J. Epidemiol. Community HealthHome page
E Malacova, J Li, E Blair, E Mattes, N de Klerk, and F Stanley
Neighbourhood socioeconomic status and maternal factors at birth as moderators of the association between birth characteristics and school attainment: a population study of children attending government schools in Western Australia
J Epidemiol Community Health, October 1, 2009; 63(10): 842 - 849.
[Abstract] [Full Text] [PDF]

Home page
 PediatricsHome page
S. Yang, J. Lynch, E. S. Susser, and D. A. Lawlor
Birth Weight and Cognitive Ability in Childhood Among Siblings and Nonsiblings
Pediatrics, August 1, 2008; 122(2): e350 - e358.
[Abstract] [Full Text] [PDF]

Home page
 Am J EpidemiolHome page
E. Malacova, J. Li, E. Blair, H. Leonard, N. de Klerk, and F. Stanley
Association of Birth Outcomes and Maternal, School, and Neighborhood Characteristics with Subsequent Numeracy Achievement
Am. J. Epidemiol., July 1, 2008; 168(1): 21 - 29.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
167/1/103    most recent
kwm245v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (3)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Leonard, H.
Right arrow Articles by Bower, C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Leonard, H.
Right arrow Articles by Bower, C.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?