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American Journal of Epidemiology Advance Access originally published online on March 8, 2006
American Journal of Epidemiology 2006 163(9):829-837; doi:10.1093/aje/kwj108
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American Journal of Epidemiology Copyright © 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

Original Contribution

Fetal Growth and Childhood Behavioral Problems: Results from the ALSPAC Cohort

Nicola J. Wiles1, Tim J. Peters2, Jon Heron3, David Gunnell4, Alan Emond5, Glyn Lewis1 for the ALSPAC Study Team

1 Academic Unit of Psychiatry, Department of Community Based Medicine, University of Bristol, Bristol, United Kingdom
2 Academic Unit of Primary Care, Department of Community Based Medicine, University of Bristol, Bristol, United Kingdom
3 Avon Longitudinal Study of Parents and Children, Department of Community Based Medicine, University of Bristol, Bristol, United Kingdom
4 Department of Social Medicine, University of Bristol, Bristol, United Kingdom
5 Academic Centre for Child and Adolescent Health, Department of Community Based Medicine, University of Bristol, Bristol, United Kingdom

Correspondence to Dr. Nicola J. Wiles, Academic Unit of Psychiatry, Department of Community Based Medicine, University of Bristol, The Grange, 1 Woodland Road, Bristol BS8 1AU, United Kingdom (e-mail: nicola.wiles{at}bristol.ac.uk).

Received for publication August 19, 2005. Accepted for publication December 13, 2005.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Using data on 4,813 children from the ALSPAC cohort in Bristol, United Kingdom, recontacted in 1998–1999, the authors investigated whether intrauterine growth restriction (indexed by birth weight and length) was associated with behavioral problems at age 7 years. Childhood behavioral problems were measured by using a brief behavioral screening questionnaire (the Strengths and Difficulties Questionnaire (parental completion)). For term singleton infants, a one standard deviation increase in birth weight was associated with an 11% reduction in the odds of behavioral problems at age 81 months. After adjustment for confounders and birth length, this association was no longer seen. The association with birth length remained after adjustment for confounders. A one standard deviation increase in birth length was associated with a 14% decrease in the odds of being in the top tertile of total behavioral difficulties at age 81 months (odds ratio = 0.86, 95% confidence interval: 0.79, 0.95) and was similarly associated with hyperactivity and conduct problems. Evidence was weak for an association between birth length and behavioral problems earlier in childhood. In summary, there was a weak association between intrauterine growth restriction, indexed by birth length (rather than weight), and childhood behavioral problems. Future work should focus on elucidating the biologic mechanisms that lead to variations in birth length and underlie this association.

birth weight; body height; child behavior; fetal development

Abbreviations: ALSPAC, Avon Longitudinal Study of Parents and Children; IQ, intelligence quotient; IUGR; intrauterine growth restriction; SDQ, Strengths and Difficulties Questionnaire


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Advances in neonatology have meant that an increasing number of children born at low birth weight (<2,500 g) and extremely low birth weight (<1,500 g) are surviving. A growing body of evidence has quantified the cognitive and educational outcomes for these children. Low birth weight is now well recognized as a risk factor for cognitive impairment in childhood (1Go, 2Go) and is also a marker for early infant mortality (3Go, 4Go). Moreover, low birth weight has been associated with depression and anxiety in adulthood (5Go–9Go). Other studies have found that low birth weight is related to childhood behavioral problems (10Go–23Go). Specifically, low birth weight has been linked with hyperactivity/attention problems (10Go, 11Go, 14Go, 16Go–23Go), externalizing (conduct problems or aggressiveness) (12Go, 15Go, 17Go, 18Go, 20Go), and internalizing (emotional problems/depression/anxiety) behavior (13Go–15Go, 17Go, 19Go, 20Go, 23Go).

However, most studies have not distinguished between intrauterine growth restriction (IUGR) and preterm delivery. Preterm infants are more likely to receive a variety of medical interventions and may experience other medical problems such as breathing difficulties that could affect outcome. Selecting children according to birth weight does not distinguish between children who are small for gestational age and those preterm infants who are in fact of an appropriate weight for their gestational age. Low birth weight can be considered a marker of impaired fetal growth only after allowing for gestation. Given that the brain is developing rapidly in utero, it is plausible that, for those infants who experience IUGR, subtle changes in brain development may influence later behavior.

There are few data to determine whether the association holds across the entire birth weight spectrum. In a population study of twins, van Os et al. (24Go) observed a linear association between birth weight and childhood behavioral problems. Likewise, using data from the 1997 Health Survey for England, Kelly et al. (25Go) found that birth weight was predictive of behavioral problems in childhood across the entire birth weight spectrum. In the latter study, no data were available on gestational age, limiting the interpretation of birth weight as a marker of fetal growth. In direct contrast, Gale and Martyn (8Go) found little evidence for a linear relation across the whole birth weight range, although boys weighing less than 2.5 kg at birth were more likely to experience psychological distress at age 16 years. Others have commented on an elevated risk of depressive disorder in late adolescence but have not distinguished between low birth weight and preterm birth (26Go). Low birth weight is only one index of IUGR, and none of the above studies examined the association between other indices of IUGR, such as birth length, and childhood behavioral problems.

Therefore, this study aimed to investigate whether IUGR (indexed by birth weight and birth length at term) is associated with behavioral problems at age 7 years. We used data from the Avon Longitudinal Study of Parents and Children (ALSPAC).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
The ALSPAC study
Data from the ALSPAC study (collected in 1998–1999) were used in the present analysis. Full details of this study have been published elsewhere (27Go) (www.alspac.bris.ac.uk). In brief, all women residing in Bristol, Avon, United Kingdom, with an expected delivery date between April 1, 1991, and December 31, 1992, were eligible to take part in ALSPAC and were enrolled during early pregnancy. Ethical approval was obtained from local research ethics committees and from the ALSPAC Ethics & Law subcommittee. For the present analysis, all multiple births and children with major congenital malformations or major illnesses were excluded from the data set, as were those for whom data on birth weight or gestational age were missing. Of the 13,474 singleton livebirths, 12,783 infants were born at term (≥37 completed weeks).

Data collection
Birth weight data were available from obstetric records. Mothers reported the date of their last menstrual period on entry to the study, from which gestational age was calculated. Where there was conflicting information regarding last menstrual period from clinical or pediatric estimates, the clinical records were reviewed, and dating was based on the earliest ultrasound scan. Birth length (crown to heel) was measured by ALSPAC staff using a Harpenden neonatometer (Holtain Ltd., Crymych, United Kingdom). Training in the use of this equipment was provided by an expert from the Institute of Child Health, London (Michael Preece, Professor of Child Health and Growth).

Data on potential confounders were available from self-report postal questionnaires completed by the mother during pregnancy or shortly after the birth of the child. Included were gender of the child, maternal smoking during pregnancy (recorded at 18 weeks' gestation: never smoked, not currently smoking but smoked before pregnancy, and current smoker (also smoked before pregnancy)), maternal age (5-year age bands, grouped at extremes (<20 and ≥40 years), parity (0, 1, or ≥2), socioeconomic markers (maternal education ("O" level = standard school-leaving qualification in the United Kingdom), below "O" level, or above "O" level), housing tenure (mortgage/owned, rented from council, other rented), household overcrowding (<1, 1, or >1 person per room), car ownership, prepregnancy body mass index (Quetelet's index: weight (kg)/height (m2) categorized as <18, 18–24.9, 25–29.9, and ≥30), maternal depression (Edinburgh Postnatal Depression Scale (28Go)) and anxiety (Crown-Crisp Experiential Index (29Go)) (at age 33 months of the child), and single-parent household. In addition, at age 8 years, ALSPAC participants were invited to attend a half-day clinic during which cognitive function was assessed by using the Wechsler Intelligence Scale for Children (WISC-IIIUK) (30Go). Intelligence quotient (IQ) scores were derived from this scale.

Measurement of behavioral problems
Mothers completed the parental version of the Strengths and Difficulties Questionnaire (SDQ) (31Go) for their child at ages 47 months (~4 years) and 81 months (~7 years). The validity and reliability of the SDQ have been reported previously (32Go). The SDQ comprises five subscales (each with five items): hyperactivity, conduct problems, emotional symptoms, peer problems, and prosocial behavior. Response options for each item are scored 0 to 2, giving scores ranging from 0 to 10 for each subscale and a total difficulties score (the first four subscales) ranging from 0 to 40. Higher scores denote more problems except on the prosocial subscale, which is reverse scored. If data were missing but at least three items for the subscale had been completed, scores were prorated (in accordance with instructions at the following website: www.sdqinfo.com/ScoreSheets/e1.pdf). Given that there may be greater error in measuring childhood behavioral problems in early life, our primary outcome was defined a priori as SDQ score at age 81 months. Behavioral problems were defined as the highest (or for prosocial behavior, the lowest) tertile for each subscale and the highest tertile for total difficulties.

Data sets
81-month outcome.
SDQ data were available for 7,725 (60.4 percent of term singleton) infants at age 81 months, and data on potential confounders were complete for 4,813 (62.3 percent) of them. In this subgroup, data on IQ (based on the Wechsler Intelligence Scale for Children) were available for 3,292 (30Go).

47-month outcome.
For 8,778 (68.7 percent of term) infants, there were SDQ data at age 7 months. Complete data on confounders were available for 5,333 (60.8 percent).

Statistical analysis
The primary analyses were conducted for term (≥37 completed weeks' gestation) infants. All analyses were performed by using Stata version 8.0 software (33Go). Mean (standard deviation) SDQ scores at ages 47 and 81 months were calculated for the entire ALSPAC cohort and were split by gender.

Logistic regression was used to examine the relation between markers of IUGR (birth weight/length) and the highest (or for prosocial behavior, the lowest) tertile of SDQ score at age 81 months. Birth weight and length were expressed as z scores (34Go). We calculated z scores by estimating the mean birth weight (or length) for each completed week of gestation, separately for boys and girls. In this paper, odds ratios and their 95 percent confidence intervals are reported and thus represent the odds of behavioral problems per standard deviation increase in birth weight or birth length. Models were adjusted initially for gender and gestational age (to further control for any effects of prematurity), then for birth length/weight, and finally for all other potential confounders. Because low birth weight has been linked with childhood cognition, and cognition in childhood has been linked with behavioral difficulties, IQ may also confound the birth weight–behavioral difficulties association. Therefore, the association was further adjusted for IQ in the subset of children for whom IQ data at age 81 months were available. This analysis was repeated for the secondary outcome, SDQ score at age 47 months.

Previous studies have found nonlinear associations between birth weight and various outcomes (e.g., schizophrenia (35Go) and cerebral palsy (36Go)). Therefore, a quadratic term for the z score for birth weight/length was included in the fully adjusted model to determine whether there was any evidence to support a nonlinear effect.

Growth in early infancy may moderate the relation between size at birth and later childhood behavioral problems, such that those children who are born small but whose growth catches up during early life may have an outcome different from those children who remain small. This possibility was explored in the subset of 3,716 children for whom height was recorded between ages 12 and 24 months. Length at birth and this later time point were standardized by using the British 1990 reference (http://homepage.mac.com/tjcole/FileSharing1.html). The interaction between birth length and later height (at ages 12–24 months) was then tested formally.

Finally, differences between those included or excluded from the various data sets were explored in terms of gender of the child, maternal age, parity, and socioeconomic markers (maternal education, housing tenure, household overcrowding, and car ownership). A weighted analysis using probability weights (37Go) was conducted to assess how these differences may have influenced the findings. The results of unweighted and weighted analyses were compared to determine whether exclusion of subjects because of missing data had influenced the study findings.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Distribution of birth weight and birth length
Among the 12,783 term singleton infants, the mean birth weight was 3.47 kg (standard deviation, 0.48 kg). Two percent of ALSPAC children (n = 238) were born weighing less than 2.5 kg. The mean birth length was 50.8 cm (standard deviation, 2.3 cm).

SDQ scores at ages 47 and 81 months
With time, SDQ total difficulties and hyperactivity scores decreased and prosocial behavior scores increased, reflecting a tendency for fewer behavioral problems with increasing age (table 1). Compared with girls, boys had higher scores for total difficulties primarily because of differences in hyperactivity scores. Girls had higher scores (indicating fewer problems) for prosocial behavior compared with boys. These differences were consistent across time and for the subset of 7,147 children with SDQ data at both time points. In general, the ALSPAC data were consistent with data representative of the British population (www.sdqinfo.com/bb1.html) (38Go), although ALSPAC participants had slightly fewer emotional and peer problems (table 1).


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  		TABLE 1. Mean (standard deviation) scores* on the Strengths and Difficulties Questionnaire at ages 47 and 81 months for children in the ALSPAC{dagger} cohort, United Kingdom{ddagger}

 
Fetal growth and behavioral problems at age 81 months
In crude analysis, and after adjustment for gender and gestational age, a one standard deviation (0.5 kg) increase in birth weight was associated with an 11 percent reduction in the odds of total difficulties at age 81 months (table 2). However, after adjustment for birth length, this association was no longer seen (odds ratio = 0.99, 95 percent confidence interval: 0.91, 1.09). A similar association with hyperactivity was also lost after adjustment for birth length. There was weak evidence for an association between birth weight and conduct problems/prosocial behavior, but, on adjustment for potential confounders and birth length, the confidence intervals spanned a wide range across the null. There was little evidence for an association between birth weight and emotional or peer problems at age 81 months.


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  		TABLE 2. Association of birth weight and birth length with childhood behavioral problems at age 81 months for children (n = 4,813 in the data set) in the ALSPAC* cohort, United Kingdom{dagger}

 
After adjustment for confounders, a one standard deviation (2 cm) increase in birth length was associated with a reduction in total difficulties at age 81 months (odds ratio = 0.86, 95 percent confidence interval: 0.79, 0.95). There was a similar association with hyperactivity and conduct problems (table 2). Adjustment for birth weight had little effect on the observed birth length associations.

There was very little evidence to support an interaction between birth length and growth during early infancy and behavioral outcomes at age 81 months (p for interactions = 0.21 to >0.99 for five comparisons). Some evidence suggested that those children who were born small but who grew during early infancy were less likely to exhibit low levels of prosocial behavior in later childhood. However, the evidence to support this finding was weak (interaction p = 0.041).

Fetal growth and behavioral problems at age 47 months
A one standard deviation increase in birth weight was associated with a reduction in behavioral problems (total difficulties, hyperactivity, conduct, and emotional problems) at age 47 months (table 3). However, this association was again no longer evident after adjustment for birth length and other confounders. In fully adjusted models, there was weak evidence to support an association between birth length and behavioral problems (hyperactivity and conduct problems). Finally, although there was some evidence for a nonlinear association for birth weight (refer to the last footnote in tables 2 and 3), this evidence was not found consistently in all analyses and should therefore be interpreted cautiously.


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  		TABLE 3. Association of birth weight and birth length with childhood behavioral problems at age 47 months for children (n = 5,333 in the data set) in the ALSPAC* cohort, United Kingdom{dagger}

 
Effect of including preterm infants on birth weight/length–behavior associations
Preterm infants were included in the data set (217 and 197 infants at ages 47 and 81 months, respectively), and previous analyses were repeated. However, associations between birth weight/length and childhood behavioral problems (at either time point) differed little (data not shown).

Differences between those included and excluded and results of weighted analyses
Children included in the data set were on average slightly heavier (mean birth weight, 3.50 kg (standard deviation, 0.46) vs. 3.45 kg (standard deviation, 0.48)) and longer (mean birth length, 51.0 cm (standard deviation, 2.2) vs. 50.8 cm (standard deviation, 2.3)) (t-test p < 0.001). Those included in the final data set with IQ data (n = 3,292) for the 81-month analysis were more likely to be girls, to be the children of first-time and older mothers, and to be from higher socioeconomic backgrounds (table 4). These differences were consistent across the various data sets (data not shown). When the various models were adjusted by using probability weights for the above differences, the conclusions remained the same (data not shown).


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  		TABLE 4. Comparison of characteristics of those children included in the 81-month analysis (for whom intelligence quotient data were available at that age), the ALSPAC* cohort, United Kingdom{dagger}

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Principal findings
Short birth length rather than low birth weight (as a measure of IUGR) was associated with more behavioral problems (in particular, hyperactivity and conduct problems) at age 81 months (~7 years). This association was observed across the entire distribution of birth length rather than being confined to infants whose growth was severely retarded. Evidence was weak for an association between birth length and hyperactivity/conduct problems earlier in childhood.

Strengths and limitations
The ALSPAC cohort is broadly representative of the population of Great Britain (27Go). The main strengths of this cohort are the large number of children studied and the detailed longitudinal data that have been collected, including information on a large number of potential confounders. The potential for recall bias in the measurement of birth weight and length is not an issue because such data were extracted from obstetric records or were based on measurements made by trained ALSPAC staff shortly after the child's birth.

Childhood behavioral problems were ascertained by parental completion of the SDQ. Reliance on parental report may underestimate conduct problems, although in comparison to data from a national survey (38Go), the mean SDQ scores were broadly similar. Any such misclassification would tend to weaken the association (with birth weight/length). While postnatal factors may be important in shaping behavior later in childhood, we found very little evidence to support a modifying role for growth in early infancy. The weaker evidence for an association between measures of IUGR and childhood behavioral problems in early life (at age 47 months) may reflect the stage of brain development. Alternatively, there may be greater error in measuring childhood behavior in the early years.

The effect size for the observed association between birth length and childhood behavioral problems was small. Although we adjusted for a large number of confounders, including maternal smoking during pregnancy, we cannot rule out residual confounding. For example, data on hypertension were not available. Importantly, we did include maternal size (height/weight) in our adjustments, and, as such, some of the genetic influences on infant size were accounted for. On the basis of previous studies, when we included preterm infants in our data set, we expected to find a stronger association between birth length and childhood behavior, but we found little such evidence. However, preterm infants are somewhat underrepresented in ALSPAC because, at the time of recruitment, those born at less than 32 weeks' gestation were recruited for a randomized controlled trial and consequently no longer participated in the ALSPAC study. This factor may explain the lack of an effect.

Data from less than half the cohort were used in the main analyses. Nevertheless, the conclusions from a weighted analysis, accounting for differences between those included and excluded from the data set, were in agreement with the results of the unweighted analysis. Exclusion of subjects from the cohort because of missing data was therefore less likely to have biased the results.

Comparison with previous studies
Many studies (10Go–23Go) have found that low birth weight or extremely low birth weight infants have more behavioral problems in childhood, but prior studies have often relied on small samples (n < 150) (11Go, 14Go–16Go, 19Go). Although others have found that the association holds across the birth weight spectrum (24Go, 25Go), contradictory evidence also exists (8Go). Furthermore, in previous studies, adjustment for confounders was limited, and no data were available on gestational age in an earlier study (25Go). Others have not separated the effects of preterm delivery and low birth weight (26Go) or, among term infants, have not examined the association across the entire birth weight spectrum (classified as above/below the 10th centile) (39Go).

None of the studies discussed above examined the role of birth length. From studies of risk factors for schizophrenia, the evidence is mixed. Three studies found no association between birth length and risk of schizophrenia (40Go), whereas others observed an increased risk for shortness (41Go) or thinness (42Go) at birth. A recent Swedish cohort study of over 700,000 individuals found that short birth length rather than low weight was important (43Go). Conflicting evidence exists for the role of birth length (vs. birth weight) in the etiology of cardiovascular disease (44Go–46Go).

Interpretation of association with birth length
The results of this study suggest that birth length but not birth weight is independently associated with childhood behavior. Both birth length and weight are measures of IUGR. There are three possible explanations for why length, rather than weight, was found to be associated with childhood behavioral problems. Firstly, there may have been less error in the measurement of birth length, which was measured by trained ALSPAC staff, whereas birth weight was extracted from obstetric records. If two variables that measure the same underlying concept (in this case, IUGR) are entered into the same regression model, there will be greater power to detect an association with the variable that is measured more precisely. However, less error in the measurement of length rather than weight is unlikely due to the greater difficulty in recording birth length as a result of infants' movement and resistance to leg straightening. Secondly, the association with birth length rather than weight may be a chance finding. Finally, proportionately, the fetus grows, in terms of length, more rapidly in the first two trimesters, whereas weight gain is greatest in the final trimester. The results may therefore point to a critical period for brain development early on in pregnancy that manifests itself in later behavioral problems.

Birth weight and birth length are both crude measures of IUGR. In the first trimester, obstetricians measure crown-to-rump length and, in the later stages, use serial measurements of head and abdominal circumference (and the ratio thereof) to identify cases of IUGR. Examining the relation between such measurements and childhood behavior may shed further light on the role of IUGR in the etiology of childhood psychopathology.

While the size of the association between birth length and childhood behavior was small, such effects are important in public health terms. Moreover, we likely underestimated the "true" effect. We hypothesize that factor(s) that affect intrauterine growth may also result in brain damage, which in turn affects later behavior. If we were able to measure those intrauterine factors affecting growth directly, the magnitude of the association with childhood behavioral problems would be larger because we would eliminate the random measurement error inherent in a proxy measure such as birth length.

Conclusions and directions for future research
IUGR early in pregnancy is associated with the emergence of behavioral problems in childhood, particularly hyperactivity and conduct problems. Subtle pathophysiologic changes during brain development may result from factors that affect growth in utero, and, as the brain develops and matures, such changes may affect childhood behavior. Alterations in the hypothalamic-pituitary-adrenal axis, growth hormone axis, and thyroid function have been proposed. Experimental work in animals provides evidence that environmental exposures early in life may result in lasting changes in hypothalamic-pituitary-adrenal activity (47Go). While future work needs to focus on elucidating the biologic mechanisms underlying such effects, this hypothesis is consistent with the fetal programming hypothesis whereby in utero exposure may result in permanent changes to metabolism and physiology that persist or emerge in later life.


   ACKNOWLEDGMENTS
 
This study could not have been undertaken without the financial support of the Wellcome Trust, the Medical Research Council, the University of Bristol, the Department of Health, and the Department of the Environment.

The ALSPAC study is part of the European Longitudinal Study of Pregnancy & Childhood initiated by the World Health Organization.

The authors are grateful to all the mothers who took part and to the midwives for their cooperation and help in recruitment. The whole ALSPAC study team comprises interviewers, computer technicians, laboratory technicians, clerical workers, research scientists, volunteers, and managers, who continue to make the study possible. The authors also thank Professor Andrew Whitelaw for his comments on an earlier draft of this paper.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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