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* Department of Developmental Paediatrics, Mater Children’s Hospital, Brisbane, Queensland, Australia
Child Development and Rehabilitation Services, Mater Children’s Hospital, Brisbane, Queensland, Australia
School of Population Health, University of Queensland, Brisbane, Queensland, Australia
|| Department of Anthropology and Sociology, University of Queensland, Brisbane, Queensland, Australia
¶ Child and Youth Mental Health Service, Mater Children’s Hospital, Brisbane, Queensland, Australia
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Methods. A total of 7388 term infants have been followed prospectively since birth. At 14 years, 5059 mothers completed a Child Behavior Checklist and provided information on their child’s school progress. A total of 5051 adolescents completed a Youth Self Report, with 3703 also undergoing psychometric testing with Ravens Progressive Matrices and Wide Range Achievement Test (WRAT) reading subtest. Outcomes were compared on the basis of birth weight groups and measures of body symmetry and were adjusted for the level of social risk at birth.
Results. Adolescents who were born small for gestational age (SGA), when compared with their appropriately grown counterparts (>10th percentile), were more likely to experience learning difficulties, with a higher prevalence in those of birth weight 
3rd percentile. Girls of birth weight 3rd percentile were more likely to have attentional problems and low WRAT reading scores. There was no significant difference in Ravens IQ or mean WRAT reading scores between SGA and non-SGA groups. There was no association between body symmetry and any of the outcomes studied.
Conclusions. SGA status seems to have only modest independent effects on learning, cognition, and attention in adolescence. Severity but not symmetry of growth restriction predicted learning difficulties.
Key Words: learning difficulties • cognition • attention • small for gestational age • symmetry
Abbreviations: SGA, small for gestational age • PI, Ponderal Index • BHR, birth weight-to-head circumference ratio • WRAT, Wide Range Achievement Test • SD, standard deviation • CBCL, Child Behavior Checklist • YSR, Youth Self Report • CI, confidence interval • WISC, Wechsler Intelligence Scale for Children
There is substantial evidence that small-for-gestational age (SGA) term infants are at increased risk for later mild cognitive deficits and behavioral problems, particularly difficulties with attention control.1–7 Not all studies, however, demonstrate this association,8–10 which may reflect the differing definitions of SGA, heterogeneous cause, and the difficulty controlling for confounding by psychosocial factors.11,12
A limited number of studies have followed SGA term infants into adolescence.13 In their Working Group report, Goldenberg et al13 concluded that most show a small but statistically significant effect of SGA status on intellectual ability (IQ) and school achievement, together with a mild increase in attentional problems and hyperactivity. They also formed the opinion that the degree of growth retardation was related to more adverse outcomes. Pryor et al1 suggested that the combination of reduced cognitive ability, problematic behavior, and short stature could potentially lead to adverse psychosocial sequelae in adolescence for SGA children. Several other studies,2,14–16 using differing definitions of SGA status, reported trends for subtle cognitive and learning difficulties in adolescence. Few studies have addressed gender differences in learning and behavioral outcomes.
Previous authors have suggested that differences in body proportionality ("symmetry") of SGA infants may reflect differences in the timing and cause of growth restriction.17–19 It has been proposed that symmetric growth restriction (whereby weight, length, and head growth all are reduced) suggests a process occurring in early to mid-pregnancy, whereas asymmetric growth restriction (with relative "head sparing") takes place in later pregnancy.19 According to this theory, brain growth is more likely to be affected by an early pregnancy process, and therefore children with symmetric growth restriction would be expected to have a higher incidence of subsequent cognitive problems and learning difficulties. Other authors have cast doubt on the concept of "brain sparing,"19 and it remains uncertain whether differences in the body proportionality of SGA infants are predictive of these adverse outcomes.20
Prevalence of growth restriction is also related to social disadvantage.21–23 As low socioeconomic status is also associated with learning and behavioral difficulties,24,25 the extent to which adverse developmental outcomes of intrauterine growth restriction are mediated by social adversity is uncertain. Evidence of a significant risk for specific subgroups of SGA children would lend support to recommendations for targeted early intervention and for increased surveillance for learning and behavioral problems in these children.14
In this study, we examined whether the presence or severity of growth restriction at full term was an independent risk factor for subsequent cognitive impairment, learning problems, or attentional deficits in male and female adolescents. In addition, we aimed to determine whether these adverse outcomes were predicted by measures of body proportionality ("symmetry") in those who were born SGA and to what degree any independent effect of SGA status was determined by social disadvantage at birth.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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37 weeks’ gestation) deliveries, with 97% of infants being of white background. Reasons for the 397 exclusions include prematurity, perinatal deaths, and adoptions. This birth cohort has been followed prospectively at 6 months and 5 years, with the most recent follow-up at 14 years of age (mean age for boys: 13.9 years [range: 12.5–15.5]; mean age for girls: 13.9 years [range: 12.1–15.4]). At the 14-year assessment, families were contacted, and 5059 mothers and 5051 adolescents (2589 boys, 2462 girls) completed questionnaires, with 3703 adolescents (1905 boys, 1798 girls) also agreeing to psychometric assessments. A comparison of birth cohort members who had behavioral assessments at 14 years with those who did not is presented in Table 1. Using similar comparisons to those in Table 1, the characteristics of the adolescents who completed behavioral questionnaires only were almost identical to those who also underwent psychometric assessment. SGA status itself; intensive care nursery admission; and having a mother who was younger, less well-educated, unmarried, or poorer all predicted loss to follow-up.
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37 weeks were subdivided into 3 groups on the basis of birth weight—3rd percentile, >3rd to 10th percentile, and >10th percentile—using Australian norms for male and female infants.27 Two measures of body proportionality (symmetry) were examined for each SGA child 10th percentile birth weight: Ponderal Index (PI) and a birth weight-to-head circumference ratio (BHR). The PI was calculated using the following formula: PI = birth weight (g) x 100/length (cm)3. The BHR was calculated as follows: BHR = birth weight (g)/head circumference (cm). Separate analyses were performed for both measures, with subjects divided into quartile groups. At birth, both head circumference and length were recorded from the medical chart as the midpoint value for each 1-cm interval. For example, head circumference values between 34.0 cm and 34.9 cm were recorded as 34.5 cm.
Outcomes
Learning Difficulty
Two measures of learning difficulty were defined. First, at the 14-year assessment, mothers completed a detailed questionnaire, which included items on their child’s school performance. These school-related questions were as follows: 1) parental impression of current school performance (graded as below average, a bit below average, average, a bit above average, or above average), 2) has the child ever repeated a school year (yes/no)? and 3) has the child ever been enrolled in a special education class (yes/no)? Learning difficulty was defined by a child’s repeating a school year, being enrolled in a special education class, or mother believing that his or her school performance was "below average." Second, those who attended for a physical assessment completed the Reading Scale of the Wide Range Achievement Test (WRAT). The WRAT 328 is an academic achievement test that has been shown to have good correlation with the Wechsler Individual Achievement Test.29 It consists of 3 subtests: reading, spelling, and arithmetic. In this study, only the reading subtest was used. A score on the WRAT reading test of <1 standard deviation (SD) below the mean (ie, <85) defined a second measure of learning difficulty. Mean WRAT reading scores were also examined.
Cognitive Abilities
Adolescents who attended for a physical assessment also completed the Ravens Standard Progressive Matrices test.30 The Ravens is a test of nonverbal intelligence with established validity and reliability.31 The test was restandardized for Australian norms in 1986.32 It is based on perceptual analogies presented in the form of 2-dimensional pattern-matching matrices in which 1 small section is missing. Children are asked to choose from 6 options the 1 that best fits the missing section. The items become progressively more difficult. A measure of nonverbal IQ is obtained (mean: 100; SD: 15). In this study, the Timed Group Administration was used.
Attention
Mothers completed a Child Behavior Checklist (CBCL)33 at the adolescent assessment. Results in this study are limited to the attentional problems subscale of the CBCL, which has been shown to have a sensitivity of 75% and a specificity of 99% for the diagnosis of attention-deficit/hyperactivity disorder.34 At the 14-year assessment, adolescents completed a Youth Self Report (YSR) questionnaire35. The YSR is a standardized self-report questionnaire for adolescents, designed to assess the same behavioral subscales as the CBCL. Children who scored in the top 10% of the attentional problems subscale on the CBCL or YSR were categorized as having attentional difficulties.
Social Variables
Maternal age, level of education, income, and marital status were measured by maternal questionnaire at the first antenatal visit. The extent to which the association of learning difficulties with SGA status was independent of potential confounding by these social factors was examined by stratifying the study group according to social risk. A Social Risk Score similar to that used by Schmidt and Wedig36 was calculated, using social risk factors present at the time of the child’s birth. Subjects were allocated 1 point for each of the following risk factors: average family income <$10 400, maternal education less than year 10, maternal age <20 years, and single parent status, with the total making up the Social Risk Score (range: 0–4 points). Subjects were then stratified into low social risk (0 points), intermediate social risk (1–2 points), or high social risk (3–4 points).
Statistical Analysis
The data were analyzed using SPSS/PC+.37 For continuous, normally distributed variables, the analysis of variance was used. The 
2 test was used for categorical data. For the stratification analysis, we defined SGA status as 10th percentile so as to include sufficient numbers of children in each category to provide stable estimates. Two-tailed P values of <.05 were considered to indicate statistical significance.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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3rd percentile being more severely affected than children of birthweight >3rd to 10th percentiles. Male infants who were born SGA experienced a higher overall prevalence of learning difficulties than female infants who were born SGA, although the relative risk of learning difficulties for SGA children, when compared with those of birth weight >10th percentile, was similar for boys and girls. Female children born 3rd percentile were significantly more likely to have a WRAT score <85, whereas there was minimal difference between the >3rd to 10th and >10th percentile groups. A similar trend was noted for boys, although differences were not significant.
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3rd percentile), 98.8 (>3rd–10th), and 100.2 (>10th). The difference in mean scores among these birth weight groups was statistically significant for girls only, where the deficit of –3.4 points (95% confidence interval [CI]: –6.5 to –0.2) for girls 3rd percentile compared with non-SGA female infants was small and of limited clinical significance. Seventy percent of those reported to have learning difficulties also scored <85 on the WRAT reading scale (P < .001). The mean WRAT reading score for those with learning difficulties (87.8) was significantly less than those with no reported problems (103.1; P < .001). The incidence of learning difficulties in those who had psychometric testing (19.8%) was almost equal to the incidence in those who completed behavioral questionnaires only (20.5%).
Cognitive Abilities
Differences in Ravens IQ scores between SGA and non-SGA groups were also of small magnitude and did not reach statistical significance for either male or female children. Mean scores on Ravens IQ test for the whole study group were 97.2 (3rd percentile), 99.9 (>3rd–10th), and 100.2 (>10th).
Attention
The percentage of male and female children, according to SGA classification, who experienced attentional difficulties as reported on the parent-completed CBCL or adolescent-reported YSR is shown in Table 2. For male children, no differences were statistically significant for either CBCL or YSR. For girls, attentional problems were reported more frequently (on the YSR) by adolescent girls who were born 3rd percentile. These differences remained significant when children with and without learning difficulties were analyzed separately. No differences in prevalence of attentional problems in girls were noted on the parent-completed CBCL. A total of 433 subjects were thought by their parents to have attentional problems, whereas 444 adolescents reported their own difficulties with attention control. Of these, only 121 adolescents were common to both groups. This low level of correspondence between the CBCL and YSR attentional problem subscales is consistent with previous reports.38,39
Symmetry
The extent to which learning difficulties, cognitive abilities, and attentional problems were related to proportionality ("symmetry") of growth restriction is shown in Table 3. Although the effect of SGA status in this study was most marked in those who were born 3rd percentile, it was necessary to examine children who were born 10th percentile in this analysis to have sufficient numbers for valid statistical estimates. Children who were born 10th percentile were subdivided into quartile groups on the basis of 1) PI and 2) BHR. For both of these measures, the proportion of children with learning difficulties and attentional problems was similar across all quartile groups, and no differences in Ravens IQ were demonstrated between the groups. For those who were born 10th percentile, the mean PI was 2.29 (SD: 0.3) and the mean BHR was 81.6 (SD: 6.8).
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10th percentile was 1.5 (95% CI: 1.3–1.8). Subjects were stratified according to their Social Risk Score into low-, intermediate-, and high-risk groups. The relative risk of learning difficulties associated with SGA status (10th percentile) compared with the reference category (those born >10th percentile) was similar within each stratum, indicating minimal evidence of effect measure modification. The unadjusted relative risk of 1.5 was similar to the stratum-specific estimates. Using a logistic regression model, with risk of learning difficulty as the dependent variable and SGA status 10th percentile and social risk category (included as 2 dummy variables with low risk as the reference category) as predictor variables, the adjusted odds ratio for SGA status 10th percentile and learning difficulty was 1.7 (95% CI: 1.4–2.1). This compares to an unadjusted odds ratio of 1.75 (95% CI" 1.4–2.1). When interaction terms between the 2 social risk variables and SGA status 10th percentile were included in the model, these were not statistically significant. The effect of SGA status on attentional problems and low WRAT scores in this study was most marked in those who were born 3rd percentile, and small numbers precluded stratification for these outcomes.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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3rd percentile for birth weight were more likely at 14 years to score below 85 on WRAT reading assessment and report attentional difficulties on YSR than their counterparts of appropriate birth weight (>10th percentile). There was no significant deficit on Ravens IQ score in adolescents who were born SGA. Measures of symmetry of growth restriction did not predict any of the above outcomes.
Previous studies of cognitive outcomes of growth-restricted, term infants have varied in definitions of SGA, age at assessment, and outcome measures used. Studies by Hawdon et al10 and Martyn et al40 failed to demonstrate any significant deficit in cognitive abilities for those who were born SGA. Several investigators have, however, demonstrated a trend for SGA children toward lower scores on cognitive indices in adolescence. Pryor et al1 examined full-term infants who were born <10th percentile and found that at 13 to 15 years, these children had Wechsler Intelligence Scale for Children (WISC) IQ scores 8 points lower on average than those of birth weight >10th percentile. In 2 studies, Paz et al14,41 examined 17-year-old recruits to the Israeli army, using 3rd percentile of their study cohort as their SGA category. Once again, there was a statistically significant trend to lower IQ scores for the SGA group, although deficits were <5 IQ points, with scores still well within the normal range. Westwood et al2 matched SGA cases (<2 SDs below hospital mean) from a previous cohort with controls of appropriate birth weight. On WISC and WRAT assessment at 16 years, there was a trend to lower scores in the SGA group, which did not reach statistical significance. Our results support the view that the risk of impaired cognitive abilities attributable to SGA status alone is mild and not clinically significant.
Our finding of an increased prevalence of learning difficulties in SGA children supports the work of several previous authors. Low et al42 used the 10th percentile as their cutoff and studied their subjects at 9 to 11 years with measures including the WRAT and Woodcock Reading test. The term SGA subjects had twice the risk of learning deficits, defined as <2 SDs below expected achievement for age. In the latest report on a large-scale prospective cohort study by Strauss,15 the SGA (5th percentile) children were assessed at 16 years and were equivalent to peers in standardized tests of vocabulary and spelling but on teacher assessment of math and overall academic performance were significantly more likely to be rated in the lower 15% of the class. Zubrick et al16 found SGA children more likely to be rated as academically impaired. Hill et al43 found a significantly increased need for special education in children who were defined as growth restricted.
Pryor et al,1 Hawdon et al,10 Walther,20 and Lagerstrom et al44 demonstrated small but significant differences between SGA children and normal control subjects in attentional problems,1,10 poor concentration,20,44 and hyperactivity/distractibility.10,44 In our study, only girls who were born 3rd percentile reported a higher prevalence of attentional problems in adolescence.
In few of the studies examining cognitive and behavioral outcomes of SGA children has consideration been given to an effect of the child’s gender. Pryor et al1 showed a larger deficit in IQ (10.3 points vs 4.9 points) and reading ability at 13 years for SGA girls compared with SGA boys. Paz et al14 found that the adjusted mean IQ was several points lower in SGA girls than in SGA boys. Lagerstrom et al44,45 found that only girls who were born SGA were at greater risk of later cognitive and behavioral problems, including concentration difficulties. In our study, we also found that growth-restricted girls were at greater risk of adverse educational and behavioral outcomes in adolescence than boys, although the differences were subtle and of limited clinical significance.
Many studies looking at outcomes of growth-restricted infants have examined children of birth weight <10th percentile.1,3,7,8,42 Other studies have focused on subjects who had more severe growth retardation than this.2,9,10,14 Goldenberg et al,5,13 in their reports on neurodevelopmental outcomes of children with intrauterine growth retardation, concluded that the degree of growth deficit seems to be a major factor in determining unfavorable outcomes. Grantham-McGregor46 suggested that, in terms of the risk for poor cognitive development for growth-restricted infants, the 10th percentile may be too high as a cutoff point. With respect to learning difficulties and attentional problems in adolescence, our study suggests that it is children who are born 3rd percentile who are at highest risk, compared with less severely affected infants.
It has been well-established that body proportionality of SGA infants exists on a continuum, with "symmetric" (equivalent reductions in growth parameters) and "asymmetric" (relative sparing of head size and length) growth restriction representing the opposite ends of a spectrum rather than 2 distinct groups.6,11,23,47 Differences in body proportionality of SGA infants may reflect differences in cause and/or timing of growth restriction.17–19 There are limited data regarding outcomes of symmetric versus asymmetric growth-restricted infants.20 Villar et al6 studied a group of term infants of birth weight <10th percentile, which they divided into low PI and adequate PI subgroups. At 3 years, the low-PI growth-restricted children performed significantly better on developmental assessment than growth-restricted infants with adequate PI. Both groups scored lower than children of normal birth weight. In a small study, Walther20 found that a group of asymmetrically growth-restricted infants (birth weight <10th percentile, low PI) were more likely to have poor concentration, hyperactivity, and academic problems at 7 years than a matched group of normally grown term infants, although there was no comparison made to symmetrically growth-restricted children. Martyn et al37 found no association between reduced cognitive function in adult life and any measure of size or proportions at birth. There was no evidence in our study that measures of body proportionality in SGA infants are predictive of cognitive abilities, learning difficulties, or attention control problems in adolescence.
Low socioeconomic status is known to be associated with both SGA status11,21–23 and adverse educational and behavioral outcomes.24,25 Few studies have had detailed measures of social environment when examining the relationship between learning and behavioral outcomes and SGA status.46 This study has demonstrated a mild, independent effect of SGA status for occurrence of learning difficulties in adolescence, which is independent of the degree of social risk at birth. This is consistent with the findings of Low et al,42 Neligan et al,3 Hill et al,43and Lagerstrom et al.45 McGee et al48 examined the relationship between SGA status and behavioral problems at high and low levels of family adversity and also found that social risk did not significantly confound the relationship between SGA status and stable behavioral problems in childhood.
In any long-term study of this nature, subject attrition is a potential source of bias. In our study, 68% completed the behavioral and educational questionnaires, although 50% of the original cohort did not have the full battery of cognitive and behavioral assessments at 14 years. The comparison of subjects who did receive full assessments with those who did not, presented in Table 1, shows that both psychosocial disadvantage and intrauterine growth retardation was associated with loss to follow-up; a degree of caution therefore is required when interpreting our results. As loss occurred differentially from those at increased social risk, the likely effect on learning difficulty is to have underestimated the contribution from these strata of Table 4 to the adjusted relative risk. Given little evidence of effect measure modification across the strata, however, this is likely to have had little effect on the findings. As other authors have noted, a continuing cycle of adverse socioeconomic factors may have a far greater negative impact on developmental outcome than most of the biological risk factors.14 In adjusting for the effect of social factors, we stratified our study group using well-established markers of social disadvantage (family income, maternal age, maternal education, single parent status) that were present at birth. Level of social risk may change over time. It is likely that environmental factors that operate after birth would have an important bearing in determining educational and behavioral outcomes. These may include relationship discord, change in relationship status, coercive parent-child interaction, parental depression/anxiety, lack of environmental stimulation, and negative parental attitude toward education. Questions for children and parents relating to the impact of learning or behavioral difficulties (eg, a child’s self-esteem, peer relationships, school disciplinary problems) would have given additional insight into the importance of these results. Imprecision in the measurements for head circumference and length at birth could lead to a small effect being missed, although the effects of ranking make this less likely for more extreme categories. The association, however, between adolescent-reported attentional problems and BHR may have become significant. We acknowledge the heterogeneous cause of intrauterine growth restriction and that different causes of SGA status may have varying effects on the developing fetus and hence different outcomes. As stated by Bakketeig et al,49 additional research is still needed to identify those causes that affect learning and behavior independent of their effect on intrauterine growth.
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CONCLUSIONS |
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FOOTNOTES |
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Reprint requests to (M.O.) Developmental Clinic, Mater Children’s Hospital, Raymond Terrace, South Brisbane, Queensland, 4101 Australia. E-mail: miocalla{at}mater.org.au
Dr O’Keeffe is currently at Caboolture Hospital, Caboolture, Brisbane, Queensland, 4510 Australia.
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REFERENCES |
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