OBJECTIVES. Our goals were to compare cognitive, language, behavioral, and educational outcomes of preterm children to term controls and to evaluate the impact of neonatal brain injury, indomethacin, and environmental risk factors on intellectual function at 12 years of age.
METHODS. A total of 375 children born in 1989–1992 with birth weights of 600 to 1250 g enrolled in the Indomethacin Intraventricular Hemorrhage Prevention Trial and 111 controls were evaluated. Neuropsychometric testing, neurologic examination, and interviews on educational needs were completed. Severe brain injury was defined as the presence of grade 3 to 4 indomethacin intraventricular hemorrhage, periventricular leukomalacia, or severe ventriculomegaly on cranial ultrasound.
RESULTS. On the Wechsler Scales of Intelligence for Children, the preterm cohort obtained a full-scale IQ of 87.9 ± 18.3, verbal IQ of 90.8 ± 18.9, and performance IQ of 86.8 ± 17.9. Preterm children obtained scores 6 to 14 points lower than term controls on all psychometric tests after adjustment for sociodemographic factors. On the Clinical Evaluation of Language Fundamentals (test of basic language skills), 22% to 24% of preterm children scored in the abnormal ranges (<70) as opposed to 2% to 4% of controls. Preterm children with and without brain injury required more school services (76% and 44% vs 16%), and support in reading (44% and 28% vs 9%), writing (44% and 20% vs 4%), and mathematics (47% and 30% vs 6%) compared with controls. Preterm children also displayed more behavior problems than their term counterparts. Severe neonatal brain injury was the strongest predictor of poor intelligence. Antenatal steroids, higher maternal education, and 2-parent family were associated with better cognition, whereas minority status incurred a disadvantage. Indomethacin did not affect intellectual function among preterm children.
CONCLUSIONS. Preterm children born in the early 1990s, especially those with severe brain injury, demonstrate serious deficits in their neuropsychological profile, which translates into increased use of school services at 12 years.
One of the challenges of modern perinatal care for preterm infants is achieving optimal survival while simultaneously limiting the rate of neurodevelopmental handicap. High grade intraventricular hemorrhage (IVH) is a complication that has been shown to contribute to long-term disabilities associated with preterm birth.1,2
Studies extending into adolescence show that preterm children, despite normal intelligence, continue to exhibit higher rates of neurodevelopmental disabilities compared with their term peers, resulting in poorer academic and social functioning and higher educational needs.3–18 The majority of these cohorts represent children born in the late 1970s and early 1980s, before the extensive use of antenatal steroids and surfactant therapy.
We have previously shown that indomethacin lowers the incidence and decreases the severity of IVH in preterm infants.19 Follow-up studies of this cohort were reassuring with regards to the safety of indomethacin on developmental outcomes.2,20,21 Furthermore, a gender-mediated effect of indomethacin on cognitive and language skills was identified.22 Preterm boys assigned to indomethacin performed better in cognitive and verbal tasks compared with preterm placebo controls.
The objective of this study was to describe cognitive, language, and behavioral outcomes along with educational placement of preterm children at 12 years of chronological age compared with term controls. The contributions of indomethacin, early neonatal insults, and later social risk factors on cognitive and verbal outcomes were examined. It was hypothesized that preterm children would continue to exhibit significant deficits on all neuropsychological domains compared with term controls, preterm boys randomly assigned to indomethacin would continue to demonstrate a benefit in cognitive and verbal skills compared with placebo preterm subjects at age 12, and severe brain injury would be the strongest predictor of long-term cognitive function.
Between September 5, 1989, and August 31, 1992, 505 infants with a birth weight of 600 to 1250 g admitted by 6 hours of age to Women and Infants' Hospital (Providence, RI), Maine Medical Center (Portland, ME), and Yale New Haven Hospital (New Haven, CT) were enrolled after parental consent to a prospective trial on early administration of low-dose indomethacin to prevent IVH. Details of the newborn protocol have been described elsewhere.19,23 Of the 505 infants, 432 did not have IVH around 6 hours, and 431 of 432 were randomly assigned to the Primary IVH Prevention Trial19; 61 infants with grade 1 to 2 IVH were part of the Secondary IVH Prevention Trial23;12 with grade 3 to 4 IVH were also offered neurodevelopmental follow-up. All are included in our total cohort. Unless otherwise specified, results pertain to the total cohort.
For the 12-year assessment, 111 term controls were also evaluated. They were recruited from the local community or selected randomly from a telemarketing list of 10000 families. Term controls were frequency-matched to the preterm group on zip code, age, gender, maternal education, and race.
The institutional review boards of the 3 participating centers approved all protocols related to the Multicenter Randomized Indomethacin IVH Prevention Trial. Informed consents were obtained from parents of all children at the 12-year visit.
Prenatal and neonatal data were retrieved from the study database. Bronchopulmonary dysplasia (BPD) was defined as oxygen requirement and abnormal chest radiograph at 28 days after birth.24 Severe brain injury was defined as the presence of either grade 3 to 4 IVH, periventricular leukomalacia (PVL), or grade 2 and above ventriculomegaly. School psychologists blinded to the participants' perinatal history conducted neuropsychological testing. Mean standard score was 100 with a SD of 15. Participants with significant impairments who could not be tested received the test's lowest standard score. Cognitive functioning was evaluated with the Wechsler Intelligence Scale for Children-III (WISC-III),25 which yields verbal and performance IQ (VIQ and PIQ), and a composite full-scale IQ (FSIQ) score. Four-factor indices are derived from the results of the subtests: the Verbal Comprehension Index provides an estimate of verbal reasoning, the Perceptual Organization Index evaluates nonverbal problem-solving skills, the Freedom from Distractibility Index measures working memory, and the Processing Speed Index appraises the rapidity to process visual information. The Peabody Picture Vocabulary Test-Revised (PPVT-R)26 was administered to evaluate receptive listening vocabulary. The rapid naming composite of the Comprehensive Test of Phonological Processing (CTOPP)27 measured efficiency of phonological information retrieval from long-term memory. The Clinical Evaluation of Language Fundamentals (CELF)28 served to examine receptive and expressive language (syntax, semantics, and verbal language memory). The Developmental test of Visual-Motor Integration (VMI)29 measured visual perception and motor planning. Reading skills were determined using the Test of Word Reading Efficiency (TOWRE)30 and the Gray Silent Reading Test (GSRT).31 In the TOWRE, participants are asked to rapidly read a list of real words and pronounceable nonwords. The task evaluates phonemic decoding and word deciphering accuracy and fluency. Finally, the GSRT taps reading comprehension. Caretakers filled out the Child Behavior Checklist (CBCL),32 a questionnaire designed to describe social competencies and emotional/behavioral issues of children. T scores above 69 (98th percentile) were considered clinically significant for behavior problems. Scores were derived for withdrawn, somatic complaints, anxious/depressed, social problems, thought problems, attention problems, delinquent behavior, aggressive behavior, and the presence of any behavior problem.
A standard neurologic examination was completed. Major neurosensory impairment was defined as the presence of any of the following: abnormal neurologic examination including cerebral palsy, hearing aids, blind services, ventriculoperitoneal shunts, or seizures. Updated sociodemographic information was provided by the primary caretakers. Details on special health care needs, school resources, and individualized educational plan (IEP) participation were collected. In the United States, an IEP is a written plan that addresses educational needs of children who struggle with their academic curriculum.
Neuropsychological outcomes were compared between preterm and term subjects (total cohort) with adjustment for potential confounders (male gender, maternal age at birth <20 years, maternal years of education, minority status by maternal report, and household structure). Between-group mean differences and odds ratio (OR) with 95% confidence intervals (CIs) were computed by using linear or logistic regression. To determine whether male gender modulated the effect of prematurity on outcomes, an interaction term between the 2 exposure factors was created. Comparative analyses between preterm and term controls were repeated after exclusion of children with severe brain injury. Multiple regression analysis was used to identify perinatal and social factors that predicted VIQ and FSIQ scores and requirement for an IEP at 12 years. Independent variables were selected based on the scientific literature. Because the primary trial was designed to examine the effect of indomethacin in preterm infants without early brain injury, analyses were repeated with restriction to the 327 children enrolled in the Primary IVH Prevention Trial to examine the treatment-by-gender effect (interaction between indomethacin and male gender). Analyses were conducted with SAS 9.1 (SAS Institute, Inc, Cary, NC).
At 12 years of chronological age, 375 preterm children were evaluated, of whom 179 (47.7%) were assigned prophylactic indomethacin. Neonatal characteristics of the 375 preterm children included gestational age of 28 ± 2 weeks (range: 23–34 weeks) and birth weight 961 ± 174 g, with 25% small for gestational age (<10th percentile). Thirty-four percent received antenatal steroids, 9% had severe brain injury, and 46% had BPD. Preterm participants and nonparticipants at 12 years were comparable with regards to gestational age, birth weight, gender, antenatal steroids, BPD, severe brain injury, maternal age at birth, minority status, and rates of neurosensory disabilities before the visit (not shown). Maternal, infant, and child characteristics of the preterm children with (n = 34) and without brain injury (n = 337) and term controls (n = 111) are shown in Table 1.
Proportions surviving were lower for preterm infants with brain injury than those with none. Maternal social characteristics were similar among all groups. Abnormal neurosensory findings were, as expected, more prevalent in the preterm cohort, especially among those with severe brain injury.
Tables 2 and 3 present the general intelligence (WISC-III), spoken and written language (PPVT-R, CTOPP, CELF, TOWRE, GRST), visual-motor coordination (VMI), and behavior (CBCL) findings. WISC-III mean IQ scores for the total preterm cohort compared with term controls are shown in Table 2. Although on average preterm children obtained IQ and factor index scores within the reference ranges, they lagged behind term controls by 9 to 14 points. The proportion of preterm children scoring in the abnormal ranges (<70) approximated 11% to 16% on the different IQ scales. IQ scores did not differ between males and females, regardless of prematurity status (not shown).
There were 337 preterm subjects available for comparisons after exclusion of preterm children with severe brain injury. Mean full-scale, verbal, and performance IQ scores for the preterm cohort without brain injury were 92.4 ± 17.3, 88.5 ± 16.5, and 89.6 ± 16.7, respectively, with 10%, 8%, and 13% scoring in the abnormal ranges. Mean differences between preterm children without brain injury and term controls narrowed, but remained significant on all scales (Table 2).
On spoken and written language testing (Table 3), the total preterm cohort consistently scored lower than the term group. Differences between the 2 were less pronounced on tests of lower-level language skills (phonological processing, phonemic (nonword) decoding and sight word reading). However, preterm subjects exhibited significant difficulties with higher-level language skills including syntax, semantics, and verbal language memory with >20% performing in the abnormal ranges on the CELF. Moreover, one quarter of preterm children obtained scores of <70 on reading comprehension.31 No interaction was identified between gender and prematurity (data not shown). The analyses were repeated with restriction to children without severe brain injury. Risk of scoring in the abnormal ranges on language testing was comparable between preterm without severe brain injury and term children on phonological processing (CTOPP; Table 3). However, preterm children without brain injury still manifested deficits compared with term controls on vocabulary, basic language and basic reading skills.
Although both preterm and term groups performed below standard references on the VMI test (Table 3), preterm children had lower scores than their term peers.
On the CBCL, preterm children (total cohort) were 5 times more likely to have at least 1 behavior problems than term controls (21.7% vs 4.7%). Figure 1 illustrates the proportion of preterm and term children scoring in the abnormal ranges on selected CBCL subscales and exhibiting at least 1 behavior problem. Parents of preterm children with brain injury reported more attention, thought and social problems than parents of term controls. Parents of preterm children without brain injury also reported increased attention deficit compared with term controls.
Table 4 displays use of educational services. Whereas 10% of term controls had an IEP, this proportion increased to 35% among preterm children without brain injury and to 76% for children with severe brain injury. A significant proportion of preterm students required additional support in reading, writing, and mathematics. Nevertheless, the majority (88%) of preterm children free of neonatal brain injury were enrolled in a regular classroom.
On multivariate linear regression, severe brain injury was the strongest predictor of verbal and FSIQs in the total preterm cohort (Table 5). Presence of this neonatal complication lead to a 20-point deficit on the VIQ and FSIQ scores. Antenatal steroids had some beneficial effect on FSIQ (3.7-point increase [95% CI: 0.3–7.1]). The remainder of the variance was in part explained by social determinants, namely maternal education (2-point increase in IQ scores for each additional year of maternal education), household structure (5-point decrease if single-parent family), and race (8-point decrease if member of a minority group). Logistic regression on requirement for an IEP showed a protective effect of antenatal steroids (OR: 0.5 [95% CI: 0.3–0.8]), whereas severe brain injury (OR: 5.2 [95% CI: 1.8–15.0]) and maternal education less than high school (OR: 2.4 [95% CI: 1.2–5.1]) increased the likelihood of having an IEP.
Indomethacin Effect in Preterm Children
All analyses were repeated to examine the effect of indomethacin on test scores among preterm children enrolled in the primary trial (Table 6). IQ scores did not differ between preterm children randomly assigned to indomethacin and those assigned to placebo. This finding remained after stratification by gender (not shown). Furthermore, there was no difference between the indomethacin and saline groups on any of the language scores. A treatment-by-gender effect was not identified. Posthoc analyses were conducted on the subset of preterm children enrolled in the primary trial who did not develop severe brain injury (n = 319) to examine the effect of indomethacin on neuropsychological outcomes. No significant differences in test scores were detected (not shown). The current study was powered at 95% to detect a 6-point difference.
In this study of neuropsychological outcomes at 12 years of age of a cohort of children born in the early 1990s, preterm children continued to lag behind term controls on all measures of intellectual function, even after exclusion of those with severe brain injury. Severe brain injury was the most important predictor of adverse cognitive sequelae. However, this study did not demonstrate a beneficial effect of indomethacin on 12-year outcomes.
Preterm children in our cohort, despite a mean FSIQ within the reference range, still scored almost 1 SD below normal term controls. Even after exclusion of children with severe brain injury, an 11-point difference remained and was clinically significant. However, the absence of serious findings on cranial ultrasound does not preclude significant brain injury that could only be visible with magnetic resonance imaging (MRI), which was not widely available during the indomethacin trial. Hence, a subset of preterm children categorized as without severe brain injury on cranial ultrasound scanning may have had unrecognized neonatal cerebral insults that could explain, among other things, the 8% to 13% rate of very low IQ scores and the 10% rate of major neurosensory impairment. In addition, other biological and environmental factors also contribute to long-term neurodevelopmental outcomes.
Almost 25% of the total preterm cohort experienced difficulties in spoken and written language comprehension as measured by the receptive component of the CELF and the GSRT. In contrast, lower level skill such as access to phonological information was almost comparable to term peers after excluding children with severe brain injury. We previously demonstrated with functional MRI that preterm children compared with term controls activated different regions of the cerebral cortex on language-based tasks at 8 years old.33 Neural pathways subserving semantic processing in preterm children were the same as those involved in phonological processing in term controls. The more preterm children exhibited patterns of brain activity similar to term controls on semantic processing tasks, the better was their verbal comprehension index score. Furthermore, indomethacin seemed to have a positive effect in preterm boys on development of brain signaling during phonological processing as the neural activation pattern was similar to term boys.34 This was not observed among preterm girls or boys randomly assigned to saline. In the current study, however, gender and indomethacin effects were not detected. Finally, imaging studies conducted on a subset of the 12-year cohort showed that preterm children engaged alternative neural pathways during phonological processing, which suggests developmental compensatory mechanisms.35 This could explain the encouraging results observed in the current study in phonological processing.
Overall, parents of preterm 12-year-old children reported more attention, thought, and social problems than parents of term controls. A number of studies have also indicated higher prevalence of anxiety and depression, withdrawn personality, and hyperactivity,3,10–14,16,36,37 which was not observed in our cohort.
Although our findings pertain to a group of children born >15 years ago, trends over time suggest that the gap in neuropsychological skills between preterm and term children has remained relatively constant.4,6,7,9,13,17 With increasing survival of children born prematurely,1,38 the prevalence of children with minor to major cognitive impairment continues to rise. This translates into a higher economic burden on the school system as illustrated by the high proportion of preterm students with brain injury (76%) and without brain injury (44%) requiring special educational services. Parents, educators, and physicians must continue to carefully monitor the academic progress of preterm teens and ensure appropriate learning supports, especially among families of lower socioeconomic status, who are at higher risk of having unmet service needs.10
Prophylactic indomethacin, which lowers cerebral blood flow in animal studies, did not adversely affect the neuropsychological outcomes at 12 years and is consistent with previous reports of this cohort at younger ages.2,20,21 A treatment-by-gender effect favoring male preterm subjects randomly assigned to early indomethacin was not identified, which suggests that the early advantage of the medication may diminish with increasing age as other variables, particularly environmental factors, become more important. As hypothesized, severe brain injury constituted the most important predictor of adverse long-term outcomes. Lower birth weight did not convey additional risk of poor cognitive performance after neonatal morbidities were added in the model. This indicates that the effect of birth weight may be mediated by associated morbidities. Contrary to other studies, we did not find lung injury to be predictive of long-term outcomes.4,6 BPD at 28 days may not have been a sufficiently sensitive measure compared with total days on oxygen or chronic lung disease at 36 weeks postconception. Our results continue to support the influence of socioeconomic factors on cognitive development with increasing age.4,18 However, we cannot distinguish at this time whether the social risks we examined directly influence IQ or are proxy measures of other indicators such as maternal IQ, quality of the home and school environment, or peer influences, which are also associated with later cognitive function.39
To our knowledge, this is the largest US follow-up study with 375 preterm and 111 term subjects to extend to 12 years of age. The retention rate of 85% was high, and the large sample size achieved allowed us to examine simultaneously the effects of multiple risk factors on outcomes. The assessment was comprehensive and covered several domains of neuropsychological abilities.
Limitations inherent to long-term cohort studies include both the lack of early MRI studies and attrition bias: children from socially and economically disadvantaged families are more likely to be lost.40,41 Therefore, our results may underestimate the true prevalence of adverse outcomes.
Preterm children manifest delays in cognitive abilities compared with term controls at 12 years of age. Severe brain injury remains a significant predictor of poor long-term outcomes, along with unfavorable social factors. Preterm survivors continue to require multiple educational supports at 12 years of age. These findings indicate that extended efforts to prevent serious brain injury in preterm infants are needed.
This work was supported the National Institutes of Health grant NS 27116.
We thank Victoria Watson, Susan Delancy, Jill Maller-Kessleman, and June Gagnon for neurodevelopmental testing.
- Accepted July 10, 2008.
- Address correspondence to Betty R. Vohr, MD, Women and Infants Hospital, Department of Pediatrics, 101 Dudley St, Providence, RI 02905. E-mail:
The authors have indicated they have no financial relationships relevant to this article to disclose.
What's Known on This Subject
Preterm children are at risk for cognitive, language, behavioral, and academic impairments. Severe IVH is associated with poorer outcomes at early ages.
What This Study Adds
Preterm children, especially those with severe brain injury born in the early 1990s, demonstrate significant neuropsychological deficits, behavior problems, and increased needs for educational support services. This is the largest US preterm cohort with comprehensive outcome data followed to 12 years.
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