Published online September 1, 2006
PEDIATRICS Vol. 118 No. 3 September 2006, pp. 1078-1086 (doi:10.1542/peds.2006-0361)
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ARTICLE

Impact of Prenatal and/or Postnatal Growth Problems in Low Birth Weight Preterm Infants on School-Age Outcomes: An 8-Year Longitudinal Evaluation

Patrick H. Casey, MDa, Leanne Whiteside-Mansell, EdDb, Kathleen Barrett, MSa, Robert H. Bradley, PhDc and Regina Gargus, MDd

a Center for Applied Research and Evaluation
b Partners for Inclusive Communities
d Division of Developmental-Behavioral Pediatrics, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, Arkansas
c Center for Research on Teaching and Learning, University of Arkansas at Little Rock, Little Rock, Arkansas


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
OBJECTIVE. The objective of this study was to assess the 8-year growth, cognitive, behavioral status, health status, and academic achievement in low birth weight preterm infants who had failure to thrive only, were small for gestational age only, had failure to thrive plus were small for gestational age, or had normal growth.

METHODS. A total of 985 infants received standardized evaluations to age 8; 180 infants met the criteria for failure to thrive between 4 and 36 months' gestational corrected age. The following outcome variables were collected at age 8: growth, cognitive, behavioral status, health status, and academic achievement. Multivariate analyses were performed among the 4 growth groups on all 8-year outcome variables.

RESULTS. Children who both were small for gestational age and had failure to thrive were the smallest in all growth variables at age 8, and they also demonstrated the lowest cognitive and academic achievement scores. The children with failure to thrive only were significantly smaller than the children with normal growth in all growth variables and had significantly lower IQ scores. Those who were small for gestational age only did not differ from those with normal growth in any cognitive or academic achievement measures. There were no differences among the 4 groups in behavioral status or general health status.

CONCLUSION. Low birth weight preterm infants who develop postnatal growth problems, particularly when associated with prenatal growth problems, demonstrate lower physical size, cognitive scores, and academic achievement at age 8. There does not seem to be an independent affect of small for gestational age status on 8-year cognitive status and academic achievement when postnatal growth is adequate.

Key Words: longitudinal study • low birth weight

Abbreviations: LBWPT—low birth weight preterm • RR—relative risk • SGA—small for gestational age • FTT—failure to thrive • AGA—appropriate for gestational age • IHDP—Infant Health and Development Program • VMI—Visual Motor Integration

Low birth weight preterm (LBWPT) infants are more likely at school age to demonstrate smaller size, more heath problems, lower cognitive skills and academic achievement, and more behavioral problems when compared with term normal birth weight peers.1–14 Term children had significantly higher cognitive scores (weighted mean difference of 10.9 IQ points) when compared with preterm children at school age in a recent meta-analysis that included data from 15 high-quality longitudinal studies.15 The average cognitive scores of preterm children were directly proportional to their birth weight. The preterm children exhibited more internalizing and externalizing behavioral problems and had more than twice the relative risk (2.64) for attention-deficit/hyperactivity disorder. It is speculated that the interaction of a broad array of prenatal and perinatal clinical features, along with a range of perinatal and postnatal environmental characteristics, may contribute to these relative deficits.16,17

The presence of prenatal growth problems (small for gestational age [SGA]) at birth or the development of postnatal growth problems (failure to thrive [FTT]) may have independent and significant effects on the broad array of negative school-aged outcomes in LBWPT children. Although the results are not uniform, a broad literature suggests that both term and preterm children who are born SGA or have intrauterine growth restriction are more likely to be smaller in size and may have lower cognitive function and academic achievement and more behavioral problems at school age than children who are born appropriate for gestational age (AGA).18–29 Likewise, children who develop FTT in the early years of life are more likely to have negative outcomes during school years.30–34 One report of a large longitudinal cohort of LBWPT children documented that almost 20% developed FTT, and these children who developed FTT had lower IQ scores and were smaller at age 3 than the LBWPT children with normal growth.35 No studies have documented the school-age status of LBWPT children who develop postnatal FTT.

LBWPT, SGA, and FTT status are interactive and confounded. A large percentage of LBWPT children are SGA, and a large percentage of LBWPT children develop FTT. In the longitudinal study of LBWPT children noted above, SGA status was the best clinical predictor to the development of FTT.35 It therefore is important to categorize LBWPT infants separately into normal growth, SGA only, FTT only, or both FTT and SGA when evaluating the differential long-term school-age status of these various conditions. In addition, various sociodemographic and socioenvironmental characteristics of families have been shown to have significant long-term effects on the array of outcomes in LBWPT or term children.21,36–39 Also, parent physical size is associated with their children's size. It therefore is important to accommodate for a variety of these features to understand the independent effect of infant growth status categories on school-age outcomes.

Limitations of school-age outcome studies of LBWPT children include small, nonrepresentative samples; single-site data; narrow array of measurement instruments; inadequate demographic data; and short-term follow-up.40,41 The Infant Health and Development Program (IHDP) is a national, collaborative, randomized, clinical trial that was conducted at 8 medical schools and was designed to evaluate the efficacy of a comprehensive intervention in the first 3 years of life in a large cohort of LBWPT children who were born in 1985.42,43 The cohort was enrolled in the nursery at 8 sites and followed in standardized study protocol until age 8. The broad array of high-quality data collected in this unique long-term longitudinal study allowed us to avoid most of the limitations in the follow-up studies of LBWPT children. We examined the following research questions: In the IHDP cohort of LBWPT infants, do infants who are AGA at birth and who do not develop postnatal growth problems differ at age 8 from those who are SGA only, have FTT only, or have FTT plus are SGA in the following: growth status (weight, height, head circumference, and BMI), cognitive status, academic achievement, behavior, and health status?


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Detailed descriptions of IHDP recruitment and subjects, study design, and intervention have been published in detail elsewhere and are reviewed briefly here.35,42,43

Sample
Infants were eligible for the IHDP study when they had a birth weight of 2500 g or less, had gestational age of 37 weeks or less, resided in the catchment area, and did not have severe medical illness or neurologic impairment. Unhealthy infants were included unless they had illnesses (eg, neural tube defects, severe sensory deficits) or neurologic dysfunction that was recognized before nursery discharge and was judged to be so severe as to preclude participation in the intervention. Only 61 such infants were excluded. The infants were enrolled from October 1984 through August 1985. A total of 985 infants constituted the primary analysis group. These infants were randomly assigned to the intervention group (n = 377) or the follow-up only group (n = 608) using a design with 2 birth weight strata: lighter (≤2000 g [n = 623]) and heavier (2001–2500 g [n = 362]). Of these original 985 infants, 71 were lost to follow-up before 30 months and were excluded from all analyses in determining the presence of FTT in the first 36 months of life.35 Infants in both intervention and follow-up groups received the same periodic medical, developmental, and social assessments through 8 years of age. The intervention program began at discharge from the neonatal nursery and continued until October 1988, when each child was at least 36 months of age, corrected for degree of prematurity. The intervention consisted of home visits (birth to 3 years), child development intervention services (age 1–3 years), and parent group meetings (age 1–3 years). At 3 years of age, the children in the intervention group had significantly higher cognitive and behavioral status and somewhat higher minor morbidity when compared with the nonintervention group.42 There were no differences in length or BMI at age 3 between intervention and nonintervention groups. By age 8, infants who were in the intervention group and had birth weight <2000 g were not different from children of the same birth weight in the control group; the preterm infants with birth weight 2000 to 2500 g showed significantly higher full-scale IQ and mathematic achievement scores.44 These difference persisted in the recently completed 18-year follow-up.45 After the intervention ended, the sites attempted to find appropriate community education programs for children in both groups before school-age entry.

Clinical Categories
SGA
Birth weight was measured by clinical staff to the nearest 10 g on admission to the nursery. Birth length and head circumference were measured with standard measuring tapes, by either project staff at the time of gestational age assessment or clinical staff on admission to the nursery. A gestational age assessment, according to the physical criteria of the Ballard Assessment, was performed within 48 hours of birth.46 SGA status was defined by weight <10th percentile on the Lubchencho Curves.47

FTT
Each IHDP site managed a follow-up clinic for clinical monitoring and research data collection. Clinical staff at each site typically included a pediatrician and a nurse clinician. Infants were weighed undressed on a calibrated infant balance scale. Length was measured in the supine position on standardized infant measurement boards, and head circumference was collected with a paper measuring tape, taking the largest measurement across the occiput and forehead. All infants were assessed at 40 weeks' postconceptual age and at 4, 8, 12, 18, 24, 30, and 36 months' gestational corrected age. Because controversy exists about the diagnosis of FTT, special consideration was given to identifying a specific case. Details of this process were described previously.35 The focus was on infants with postnatal growth deficiency as measured by poor weight gain, rather than stunting (symmetric and small in weight and length). Therefore, children were required to have lower-than-average weight growth velocity to meet criteria. Cases included infants who met all 3 of the following criteria between 4 and 36 months' gestational corrected age: (1) coded by a developmental clinician during an IHDP clinic health assessment as having FTT, (2) weight less than the fifth percentile for gestational corrected age at 2 or more points in time, and (3) rate of weight growth during the preceding months less than average for gender and gestational corrected age as determined by incremental (velocity) growth curves. In addition, infants who were not coded by the developmental clinicians as having FTT at a health assessment but met criteria 2 and 3 at 2 or more points in time between 4 and 36 months' gestational corrected age and whose blinded reviews of their growth curves by 2 developmental pediatricians led to a consensus diagnosis of FTT were coded as cases with FTT. Using these criteria, 180 infants were identified as having FTT.

Requirement of clinician concurrence on the diagnosis of FTT, low weight on >1 occasion, and lower-than-average growth velocity intentionally excluded infants who may have experienced brief decline in growth related to acute illness or other causes. This definition also excluded infants who were born SGA and who had either average or "catch up" growth velocity during postnatal life. This definition of FTT was believed to be conservative in that it required unusually low weight for corrected age, a decreased rate of growth, and clinician judgment that the child was experiencing FTT. In a blinded review of 40 growth curves by 2 developmental pediatricians, no infants who were counted as cases of FTT by study criteria were coded normal by the pediatricians, indicating a high degree of specificity for these criteria.

Of the original 985 in the primary analysis group, 874 (89%) were evaluated at 8 years of age. The percentages of children within the intervention and follow-up only groups were similar, both overall and within sites.44 We excluded 145 children from these analyses, 2 because we could not confirm SGA status and 143 who met some but not all our case criteria for FTT. These 143 children were excluded so that children who clearly experienced FTT could be compared with children who did not. Of the 840 remaining children, another 185 were excluded because of missing data, leaving 655 children for analyses. The most common variables missing were maternal height and weight; other variables missing were child Developmental Testing of Visual Motor Integration (VMI), Child Behavioral Checklist, and child General Health Survey. We compared the children who were included in the study (n = 655) with those who were excluded because of missing data (n = 185) by all baseline characteristics that were used as control variables (birth weight, gender, ethnicity, maternal education, maternal height, maternal weight, and infant intervention group), the infant postnatal growth group, and developmental and behavioral status as evaluated in the first 3 years of life. There were no differences in any of these variables except that children who had FTT but were not SGA were slightly more likely (P = .02) to be included. No other differences were seen in the above variables. We also compared the 143 children who were excluded because of uncertain growth status with those who were excluded because of missing data and those who were included in the study on the same set of baseline control variables and 8-year developmental and behavioral status variables; no differences were found.

Eight-Year Status Measures
The cognitive, academic achievement, and behavior evaluations at 8 years of age were performed by trained assessors who were masked to child's treatment group and history. Health status was assessed by clinic staff who had access to the child's treatment group assignment and history. The following measures were used for the current analyses:

  • Growth: weight (kilograms), height (centimeters), head circumference (centimeters), and BMI (kilograms divided by meters squared)
  • Health: Child General Health Survey (General Health and Physical Function and Mental Health Scales)48
  • Behavior: Child Behavior Checklist49
  • Cognition: Wechsler Intelligence Scale for Children III,50 VMI,51 and Peabody Picture Vocabulary Test–Revised52
  • Academic achievement: Woodcock Johnson Test of Academic Achievement Revised (Broad Math and Broad Reading)53

Analysis
Comparative analyses among the 4 growth groups (normal growth, SGA only, FTT, and SGA plus FTT) were performed on all 8-year status measures with multivariate analyses of variance for qualitative measures and {chi}2 test for categorical measures. After these initial comparisons, multivariate analyses (analysis of variance and logistic regression) were performed controlling for children's birth weight, gender, and ethnicity; maternal education, height, and weight; and infant intervention group assignment. Bonferroni corrections were applied to all comparative analyses. The final sample included all 655 children with the complete 8-year data required for these analyses.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Baseline demographic and growth data are shown among the 4 growth groups in Table 1. There were no significant differences among the groups' gender, maternal education, or infant intervention group assignment. There were significant differences in birth weight among the groups. Those in normal growth group were significantly heavier at birth than the SGA only and the FTT/SGA groups. The FTT/SGA group was lighter at birth than the normal and the FTT only groups but not the SGA only group. The FTT/SGA group and the FTT group were not more premature than the normal growth group. As measured by the Neonatal Health Index (calculated on the basis of length of stay in the nursery, adjusted for birth weight, and standardized to a mean of 100, the higher scores indicating better health),54 the FTT/SGA children were less sick when compared with the normal growth group. Mothers of children in the normal growth and SGA only group were taller than mothers of children in the FTT group. Mothers of children with FTT, regardless of whether they were SGA, were lighter than mothers of children in the SGA only group but not mothers of children in the normal growth group. Mothers of children in the SGA only group were more likely to be black.


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  		TABLE 1 Baseline Characteristics by Infant Growth Group

 
Weight, height, and head circumference at age 8, adjusted for baseline variables, are depicted in the Fig 1 by infant growth groups. There is a stepwise pattern noted in all growth variables, with the smallest seen in the FTT/SGA group, then the FTT group, followed by the SGA only group, and the normal growth group. The differences in most variables are clinically impressive. For example, the 8-year weight of the infants in the FTT/SGA group was 6.2 kg lighter than the normal growth group. The 8-year height of children in the FTT/SGA group was 6.8 cm shorter than the normal growth group, and the head circumference was 2 cm smaller.


Figure 1
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  		FIGURE 1 Eight-year growth status by infant growth group adjusted for baseline variables (adjusted for infant birth weight, gender, race; maternal race, education, height, and weight; and infant intervention group status). Hgt, height; HC, head circumference.

 
The 8-year growth, health, and behavior statuses by infant growth group status, adjusted for all baseline variables, are shown in Table 2. There is a stepwise progression with those in the FTT/SGA group being the smallest followed by FTT only, and then SGA only; the normal growth group was the largest in most growth variables. Each category differs significantly from the other except for FTT/SGA versus FTT only in weight, height, head circumference, and BMI; SGA versus normal growth in BMI; and SGA versus FTT only in head circumference. When BMI percentiles were calculated for age and gender, children who had FTT (particularly the FTT/SGA children) were more likely to be <10th percentile and less likely to be >85th percentile. The children in the FTT/SGA group were significantly lower on the Physical Function Scale than the children in the SGA group. There were no differences across the 4 groups in the Child Behavior Checklist, the total General Health Survey, or the Mental Health Scale of the General Health Survey.


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  		TABLE 2 Growth and Health Behavior Status at 8 Years by Infant Growth Group Adjusted for Baseline Variables

 
Eight-year cognitive/developmental status, adjusted for baseline variables, is shown in Table 3 by infant growth status. In most variables, children in the FTT/SGA group scored the lowest, followed by FTT only. The SGA only and the normal growth groups scored the highest and were very similar. The FTT/SGA group scored significantly lower than the normal and the SGA groups in the Wechsler Intelligence Full Scale and Performance Scale and the Peabody Picture Vocabulary Test. Seven percent of the FTT/SGA group had full-scale Wechsler Intelligence Scale for Children IQ score >2 SDs from the mean, compared with 1.9% of the normal growth group. The FTT/SGA group scored lower than the SGA only group on the Broad Math Achievement Test and lower than the normal growth group on the Broad Reading Achievement Score at a level that was nearly statistically significant. The FTT/SGA group was significantly lower than the normal growth group on the VMI. The SGA only group did not differ from the normal growth group in any variable.


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  		TABLE 3 Developmental Status at 8 Years by Infant Growth Group Adjusted for Baseline Variables

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
In this large, multisite, longitudinal cohort of LBWPT infants, differential outcomes at age 8 were found in physical size, cognitive status, and academic achievement but not in behavioral status among the 4 growth groups. In general, children who had both prenatal (SGA) and postnatal (FTT) growth problems were the smallest in all growth variables at age 8, and they also demonstrated the lowest cognitive and academic achievement scores. These all were significantly lower than that of children in the normal growth, except the Woodcock Johnson math score, which was significantly lower than that in the SGA only group. The children in the FTT only group were significantly smaller than the children in the normal growth group in all growth variables and had significantly lower full-scale, performance, and verbal IQ scores. The children with FTT only were somewhat larger than the FTT/SGA group in all growth variables, and they had somewhat higher cognitive and academic achievement scores, but these did not reach statistical significance. Children in the SGA only group were larger than the children in the FTT/SGA and FTT only groups in almost all growth variables, and they were significantly smaller than those of the normal growth group in all growth variables except BMI. However, the SGA group did not differ from the normal growth group in any cognitive or academic achievement measure. The SGA group scored significantly higher than the FTT/SGA group in full-scale and performance IQ and math achievement.

Most long-term follow-up studies of LBWPT infants categorize the infants by birth weight category, including very low birth weight or extremely low birth weight, or by extreme prematurity.4–14,55–60 These studies consistently demonstrate lower physical size, cognitive skills, and academic achievement in these infants when compared with normal birth weight control subjects. Most of these long-term studies have a relatively narrow focus of outcome, such as health, behavior, or cognitive/academic skills. Other studies focus on the long-term status of LBWPT children who experienced neonatal morbidities, such as bronchopulmonary dysplasia, or who received certain treatments during their nursery stay.39,61–67 As noted earlier, many have focused on the differential long-term outcomes of children who were born SGA versus AGA, with various results. To our knowledge, only 2 studies have evaluated neurodevelopmental outcome in a cohort of LBWPT infants on the basis of both neonatal growth status and postnatal growth status. In a single-site study, infants with birth weight <1250 g were followed until age 2.68 Both the AGA and SGA children who demonstrated postnatal growth concerns had significantly lower mental or physical development than those who had normal postnatal growth. The authors concluded that postnatal growth patterns, rather than SGA status, was significantly associated with adverse neurodevelopmental outcomes at age 2. Furthermore, they concluded that SGA status becomes a predictor of poor outcomes only when it is associated with significant postnatal growth problems. Hack et al69 examined at 21 months of age a group of LBW infants who had birth weight ≤1500 g. Both AGA and SGA infants who were small at 21 months had significantly lower developmental status when compared with similar infants who were normal in size. Our results further emphasize the association of postnatal growth on school-age physical size and intellectual status and academic achievement, whether the LBWPT child is born AGA or SGA, even after controlling for important maternal and child characteristics.

Ours is the first study that allows evaluation of a broad array of outcome variables into school years in a cohort of LBWPT infants on the basis of prenatal or postnatal growth status. The IHDP cohort provided many methodologic strengths, including infants' being born in 8 communities, a broad array of family demographic characteristics, and high-quality data collected in research protocol longitudinally over 8 years. This allowed placement into postnatal growth categories that follow-up studies with broad interval of data collection are not able to do. Despite the benefit of this sample, the generalizability of our sample is somewhat restricted because, as a result of the low number of extremely low birth weight infants, this sample is best categorized as a low-risk group of LBWPT infants by contemporary standards. In addition, 65% of the original primary analysis group and 73% of those who were evaluated at age 8 had all data required for analyses. One can only speculate about the affect that the loss of those subjects had on the results. However, comparative analyses of participants versus those who were excluded for missing data showed no significant differences in the control variables, the infant growth category, or early developmental status. Also, some of the maternal or infant exclusion criteria, such as maternal drug abuse or infants who required oxygen supplement for >90 days, may have excluded infants who may have been at greater risk for postnatal growth problems. Finally, no normal birth weight term infants were available in this cohort for comparison.

Most research that evaluates the follow-up growth of LBWPT infants, whether AGA or SGA, has focused on whether catch-up growth occurs and the timing of this catch-up growth.11–14,69–73 Although little research has focused on postnatal catch-down, or postnatal growth failure (FTT), the typical clinical approach to LBWPT infants has been to urge enhanced nutrition to facilitate this catch-up growth so that LBWPT infants might achieve normal physical size.74 Conversely, there has been recent concern that LBW status, whether AGA or SGA, and excessive weight gain early in life increase the probability of adult obesity, diabetes, and cardiovascular disease.75–79 However, several population-based studies found that low weight gain in the first year of life is associated with greater risk for coronary heart disease.81–83 Still, the notion of "beneficial undernutrition" is gaining interest as a potential benefit to long-term adult disease.84 In this context, our results demonstrate the association of postnatal growth problems to school-age size, cognitive skills, and academic achievement and emphasize the importance of monitoring growth in the early years of life of LBWPT infants. Future intervention research is required to determine the desired rate of growth, whether nutritional interventions can normalize postnatal growth of LBWPT infants while avoiding excessive or too rapid catch-up, and whether these interventions might modify long-term neurodevelopmental status while avoiding adult chronic diseases.74,84


   CONCLUSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Postnatal growth problems (FTT), particularly when associated with prenatal growth problems (SGA), are associated with lower physical size, cognitive scores, and academic achievement at age 8. There does not seem to be an independent effect of SGA status on 8-year cognitive status and academic achievement when postnatal growth is adequate. Although it is not clear whether aggressive clinical management of postnatal medical, nutritional, and social issues can normalize postnatal growth and improve long-term neurodevelopmental outcomes, our results emphasize the importance of considering postnatal growth status when assessing the long-term course of LBWPT infants.


   ACKNOWLEDGMENTS
 
The participating universities and site directors in the IHDP were as follows: Patrick H. Casey, University of Arkansas for Medical Sciences (Little Rock, AR); Cecelia M. McCarton, Albert Einstein College of Medicine (Bronx, NY); Michael W. Yogman and Marie C. McCormick, Harvard Medical School (Boston, MA); Charles R. Bauer and Keith G. Scott, University of Miami School of Medicine (Miami, FL); Judith Bernbaum, University of Pennsylvania School of Medicine (Philadelphia, PA); Jon E. Tyson and Mark Swanson, University of Texas Health Science Center at Dallas (Dallas, TX); Clifford J. Sells and Forrest Bennett, University of Washington School of Medicine (Seattle, WA); and David T. Scott, Yale University School of Medicine (New Haven, CT).


   FOOTNOTES
 
Accepted May 3, 2006.

Address correspondence to Patrick H. Casey, MD, 800 Marshall St, Slot 512-26, Little Rock, AR 72202. E-mail: CaseyPatrickH{at}uams.edu

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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