OBJECTIVE: To study outcome of low-risk moderately preterm birth between 32 and 36/7 weeks' gestation.
METHODS: 377 Moderately preterm children (M: 34.7, SD: 1.2 complete weeks), without need for neonatal intensive care and without dysmaturity or congenital malformations, were compared with 182 term children and assessed at eight years (M: 8.9, SD: 0.54). School situation, IQ, sustained attention, behavior problems, and attention-deficit/hyperactivity characteristics were studied.
RESULTS: Special education was attended by 7.7% of the moderately preterm children, more than twice the rate of 2.8% in the general Dutch population of this age. Additional exploration for two preterm subgroups of 32 to 33 versus 34 to 36 weeks' gestation showed a need for special education in 9.7% versus 7.3% and a significant difference in grade retention for 30% versus 17%, respectively. Of the children attending mainstream primary schools, grade retention was found in 19% of the preterm versus 8% of the comparison children. Adjusting for maternal education, a group difference of 3 points was found in IQ. The preterm children needed more time for the sustained attention task. The preterm children had more behavior problems (specifically internalizing problems with 27% scoring above the borderline cut-off), as well as more attention-deficit/hyperactivity disorder characteristics (specifically attention deficits).
CONCLUSIONS: Cognitive and emotional regulation difficulties affect functioning of moderately preterm children, as school problems, a slightly lower IQ, attention and behavioral problems are found when they are compared with term-born children. Identification and monitoring of precursors of these problems at younger age is needed in view of prevention purposes.
A moderately preterm birth between a gestational age of 32 and 36/7 weeks occurs in 9% of all births in the United States and 6.3% of all births in the Dutch population, around 11000 children per year.1,2 An increase in these rates was found between 1992 and 2003.2 Most of these moderately preterm infants survive with declining mortality rates.3 Information on development of moderately preterm children is scarce, despite the large prevalence and the potential risk for immature brain development. At 34 weeks of gestational age, the overall brain weight is only 65% of brain weight at 40 weeks.4 Potential brain damage as a result of premature birth can occur during the last weeks of gestation to term age in the structural maturational processes of the brain, which include increasing neuronal connectivity, dendritic arborization, increase in synaptic junctions, and maturation of neurochemical and enzymatic processes.
Previous reports on outcomes have used various definitions for overlapping gestational ages, with some studies describing infants of 35 to 36.6 weeks' gestation as near term and other studies describing infants of 34 to 36 weeks' gestation as late-preterm.5 In respect to neonatal outcomes, it has been found that infants born at 35 to 36 weeks' gestation have more medical problems compared with term infants.6 Preschool readiness testing in Florida showed that 13.6% of late-preterm children versus 11.8% of term children required special education at 5 years of age.7 In the United Kingdom, 7% of 7-year-old children born between 32 and 35 weeks' gestation needed special education and 19% had an abnormal hyperactivity score.8 Danish registers showed that 37 (6.4%) of 581 children between 2 and 18 years of age who were born between 34 and 36 weeks' gestation had a hyperkinetic disorder.9
In this study, the cognitive performance and socioemotional functioning of moderately preterm and term-born children at school age was compared.
Selection criteria for the preterm children consisted of: a gestational age at birth of 32 through 36 weeks + 6 days, no dysmaturity (<P10), no NICU admittance needed (uniform criteria for admission to a NICU were used by all hospitals based on official guidelines from the Dutch Society for Obstetrics and Gynecology and the Dutch Pediatric Association), no severe congenital malformations, and an age of 7 to 9 years. For the term children, the selection criteria were: gestation of ≥37 weeks, no dysmaturity (<P10), no NICU admittance needed, no severe congenital malformations, attending a primary school, and an age of 7 to 9 years.
All parents completed a background information questionnaire concerning school situation of the index child, family circumstances and lifestyle during pregnancy, and delivery characteristics. Neonatal data of the preterm children were collected from the hospital files. The parents of the term children answered a questionnaire regarding their children's neonatal characteristics. Cognitive abilities of the children were assessed with the Revised Amsterdam Children's Intelligence Test (short version) for children 4 to 11 years of age.10 The norm score (IQ score) is 100 (SD: 15) and the mean for the subtests is 15 (SD: 5). A correlation of .81 was found with a Dutch version of the Wechsler Intelligence Test–Revised.10
To measure sustained selective attention, the Bourdon-Vos test was used.11 The children are required to mark configurations consisting of 4 dots as quickly as possible, in 33 rows of 24 figures of 3, 4, or 5 dots. Psychometric properties of the test were found acceptable by the Dutch organization that provides information on Dutch psychological tests and questionnaires.12
Both parents and teachers were asked to complete a questionnaire on competences and behavior problems of the child; the Child Behavior Check List (CBCL) was filled in by the parents and the Teacher Report Form (TRF) by the teachers.13 The CBCL and TRF are parallel forms of the same questionnaire with good psychometric qualities.13 CBCL scoring provides an assessment of the total number of behavior problems, as well as separate scores for internalizing and externalizing behavior problems. A total score of 60 indicates a cutoff score for children with many behavior problems, as was found for 15% of the norm population. The CBCL also provides specific subscale scores for anxious/depressed behavior, physical complaints, social problems, thought problems, attention problems, and aggressive behavior.
In addition, parents and teachers answered a questionnaire on symptoms of attention-deficit/hyperactivity disorder (ADHD) of children aged 4 to 18 years.14 This questionnaire provides both a total score, as well as subscale scores for attention deficit, impulsivity, and hyperactivity. The validity, sensitivity, and reliability of the test are acceptable.12
Information on school outcome, that is, attending a grade appropriate for age, grade retention, or attending a school for special education, was obtained either from the parental background questionnaire or from the CBCL and TRF questionnaires.
The participating preterm children were born between January 1996 and January 1998 in 1 of the 7 participating general hospitals in the south of the Netherlands. The preterm children were selected on the basis of the hospitals' archives and their parents were invited to participate.
The term children were pupils of mainstream primary schools in the same geographical region and born between January 1996 and January 1999. Primary schools were approached in the cities where the hospitals are located, as well as in surrounding villages. First, a request to the directors of these schools was made for their school's participation. Next, the children were given a letter for their parents, which explained the study and requested their participation. If the parents gave their written informed consent, their child was tested in the hospitals or schools by examiners who each tested only preterm or only term children. The study was approved by the Committee of Medical Ethics of the St Elisabeth Hospital in Tilburg and by the committees of the other participating hospitals.
In total, 270 preterm children who were eligible for the study were not included, because they could not be located (42%), could not be studied within the time frame of the examiners (34%), their parents refused participation (5%), or the exact reason for nonparticipation was unknown (19%). The 377 participating preterm children did not differ in gestational age (34.7 weeks [SD: 1.2] vs 34.8 weeks [SD: 1.2]) or birth weight (2425 g [SD: 455] vs 2422 g [SD: 426]) from the nonparticipants. The participants also did not differ from the nonparticipants in way of delivery (82% vs 79% for vaginal delivery, respectively) and (18% vs 21% for cesarean delivery, respectively), occurrence of hypoglycemia (13% and 17%, respectively), nor in their need of any oxygen after birth (23% vs 18%, respectively). However, the participants had had phototherapy more often (43% vs 31%, χ2) = 8.79; P < .001), they were discharged from the hospital 2 days sooner (13.6 [SD = 9.0] vs 15.7 [SD = 10.0], t1,586 = 2.61; P < .01), and they were less frequently part of multiples (22% vs 36%, χ2 = 14.4; P < .001).
The distribution of 32, 33, 34, 35, and 36 completed weeks of gestation in the participating preterm group consisted of 6%, 11%, 20%, 28%, and 36%, respectively. Birth weight was <2500 g in 56% with 2 cases <1500 g.
In Table 1, the basic neonatal and demographic characteristics are presented of the term and preterm participants. The characteristics for the subgroup of preterm children, with those attending special education excluded, are presented separately. The preterm participants (both the total and the subgroup) differed as expected from the term children in birth weight, gestational age, duration of stay in the hospital, and number of multiples. The preterm infants were not more frequently born by cesarean delivery (18% vs 13%). No group differences were found in the retrospective reports of any maternal smoking (18% vs 13%), but report of any alcohol use during pregnancy (8% vs 16%, χ2 = 7.10; P < .01) was higher in the term group. The number of mothers and fathers who had completed higher education was lower in the preterm group (see Table 1). Hence, the analyses comparing functioning of the preterm group to the term group were adjusted for maternal education.
In respect to school outcome, it was found that 29 (7.7%) of the participating preterm children attended a school for special education compared with 2.8% of the Dutch population of this age group.15 Grade retention of the children attending mainstream primary schools was found in 19% of the preterm group, a significant difference from the 8.8% in the term group (χ2 = 9.45; P < .01).
In Table 2, data are presented of the IQ test, excluding the preterm children attending a special school. The multiples did not differ from the singletons and had the same mean IQ scores in the preterm group, hence no adjustments were made in this regard. The comparisons between the preterm children and the term children are presented, adjusted for maternal education. With IQ, a small group mean difference of 2.86 (SE: 1.37) was found (F1,495 = 4.38; P = .037). The groups also differed over all subtests (F6,490 = 2.59; P = .018), specifically in “idea production” (F6,488 = 6.18; P = .013), that requires the child to name as many products of a certain category as possible within 1 minute and assesses verbal associations and ideational fluency (eg, “What can you put into your pocket?”) and marginally in “hidden figures” (F6,490 = 3.65; P = .057), which assesses perceptual reasoning (pattern recognition, matching, visual distractibility, and visual analyses) of the children.
The Bourdon-Vos test showed a group difference in sustained attention to the disadvantage of the moderately preterm children, adjusted for maternal education: (F1,494 = 15.5; P = .000) (see Table 2). The preterm children (M: 19.7 seconds, SD: 4.8) needed 2 seconds more to complete a line than the term children (M: 17.6 seconds, SD: 3.22), which was a significant difference (F1,494 = 21.4; P = .000).
According to the mothers (F3,484 = 4.09; P = .007), fathers (F3,423 = 2.64; P = .049), and teachers (F3,447 = 2.81; P = .039), the preterm children had more ADHD characteristics, as analyzed with a multivariate analyses of variance adjusted for maternal education over all 3 subscales. Mothers of preterm children reported more attention deficit and hyperactivity, whereas their teachers noted only more attention deficit problems (see Table 3). Fathers' reports showed no group differences for the separate scales. Strong correlations were found for the total ADHD rating of mothers and fathers (r = 0.69) and for mothers and teachers (r = 0.60).
The groups also differed in behavior problems on the CBCL and TRF according to their mothers and their teachers; the fathers did not note group differences (see Table 3). The differences most clearly appeared in internalizing behavior problems. According to the mothers, 27% of the preterm children scored >60, the borderline cutoff score, versus 17% in the term group for internalizing behavior (χ2 = 6.34; P < .05); respectively, 16% and 12% scored above borderline for externalizing behavior, a nonsignificant difference. In respect to the specific CBCL subscales, mothers assessed the preterm children higher in the anxious/depressed, physical complaints, social problems, thought problems, attention problems, and aggressive behavior dimensions, but not in the withdrawn/depressed and rule-breaking dimensions (data not shown). Fathers' ratings did not differ for any of the dimensions. The teachers assessed significantly more behavior problems in the preterm children in the anxious/depressed, physical complaints, and social capacity dimensions.
Assessments of mothers and fathers for the total problem score correlated strongly (r = 0.55) and moderately for the mothers and teachers (r = 0.43).
Neonatal Characteristics and Subgroups in Relation to Outcome Measurements of All Preterm Children
Logistic regression analyses employing “need for special education” as a dependent variable and gestational age, birth weight, duration of hospital stay, hypoglycemia, need for oxygen, and phototherapy as predictors demonstrated a significant effect for duration of hospital stay (Exp[B] = 1.044 [95% confidence interval: 1.007–1.082]); P = .019), with a mean of 19.2 days (SD: 13.1) in the special education group versus 15.3 (SD: 9.7). Using grade retention as the dependent variable, no relationships were found with these predictors.
For IQ scores in relation to completed weeks of gestation, we found that the 21 children with a gestational age of 32 weeks differed with a mean IQ of 96 (SD: 14.5) from the later-born preterm children (mean IQ scores varying from 102–104). Comparisons of gestational age subgroups (32 to 33 weeks [n = 62] vs 34 to 36 weeks [n = 315]) showed no differences in outcome regarding special education (9.7% vs 7.3%, χ2 = .412; P = .521). These subgroups did differ in grade retention, which was 30% in the youngest group and 17% for the late-preterm subgroup (χ2 = 5.46; P < .01). Multivariate analysis of variance corrected for maternal education on all outcome measurements showed only 1 difference: the CBCL assessment of the mothers indicated more behavior problems in the late-preterm subgroup (F1,274 = 5.59; P = .019). Outcome of the preterm children on all measurements did not differ in relation to need for oxygen (23%, F8,228 = 1.23; P = .28), or phototherapy (43%, F8,262 = 1.36; P = .22) or hypoglycemia (13%, F8,217 = .678; P = .71).
More than twice as many moderately preterm born children attend special education schools compared with the registration for the general Dutch population.15 This finding, in itself, indicates a relatively large amount of cognitive or behavioral problems for the preterm group.
Although the moderately preterm children who attended mainstream primary schools at 7 to 9 years of age are functioning relatively well, they still differ from their term-born peers. Overall the results show a pattern of subtle but clear differences to the disadvantage of the moderately preterm children. These children have repeated a grade more often, indicating learning or adaptation problems. A slightly lower mean IQ of 3 points is found for the preterm children, which is not considered a clinically relevant difference. However, they also show more difficulties in the sustained attention task. Their mothers assess more behavior problems, except for the impulsivity dimension of the ADHD rating and the withdrawn/depressed and rule-breaking dimension of the CBCL. In addition, the teachers of the preterm children also report more attention deficits and internalizing problems, specifically regarding anxious/depressed behavior, physical complaints, and social capacities. The fathers of the preterm children rate their children somewhat higher on the ADHD characteristics, but their ratings of both groups do not differ in more specific dimensions of behavior problems.
When exploring the importance of neonatal characteristics, it was found that the children born at 32 weeks' gestation had a 6 to 8 points lower IQ compared with the later-born preterm children. Furthermore, a longer duration of hospital stay, with a mean of 4 days, was found in the children requiring special education. Dividing our preterm sample into 2 subgroups of 32 to 33 versus 34 to 36 weeks' gestation showed a clear difference in grade retention to the disadvantage of the youngest group. These preterm subgroups did not differ in the other outcome measures, except for more behavior problems assessed by mothers in the late-preterm subgroup. Consequently, the late-preterm children are also at risk, although the risk for problems in developmental outcome is somewhat higher in the shortest gestational age subgroups.
The findings of our study of 8-year- olds show almost the same percentage of children needing special education as found in a similar study on 5-year-olds from the United Kingdom.8 School outcome of the preterm children (32–36 weeks' gestation) in the Early Childhood Longitudinal Study-Kindergarten Cohort from the United States indicated a higher need for special education services, varying from 10.1% to 11.3% in the 32 to 33 weeks' gestation subgroup and 9.3% to 9.7% in the 34 to 36 weeks' gestation subgroup, in comparison with 9.4% to 9.7% in the term group.16 Although hyperactivity was found in 2 studies,8,9 our study indicates more internalizing problems of the preterm children, specifically attention difficulties.
The attention difficulties of the moderately preterm children indicate regulation difficulties that may underlie their cognitive and behavioral problems. The disturbance in early brain development because of premature birth and its associated treatment may have contributed to this outcome, as well as the underlying causes of premature birth or (epi-)genetic processes. More specific neonatal problems may have affected the children's brain development, but only gestational age and duration of hospital stay showed direct relations with outcome measures.
Information on the neonatal treatment and diagnoses of these moderately preterm children could not be collected in greater detail. The hospitals varied in their data collection and only 1 had computerized records. However, it is important to note that none of the children had been seriously ill and no intensive care treatment was needed. Recovery from preterm birth, as well as feeding difficulties, may have affected brain development. In addition, the bonding and interaction processes between parents and infants may have affected their development. The lower level of parental education may also have influenced the stimulation of the children.
The analyses reported are adjusted for the difference in maternal education, which may be a form of overcorrection. Moderate prematurity may in itself be associated with maternal education, in that higher educated women may better adjust their lifestyle to their pregnancy, or may seek help more efficiently in case of signals of premature labor.17
Clearly, the developmental outcome of our moderately preterm born children without need for neonatal intensive care treatment is much better than the results found for very preterm children with a gestational age of <32 weeks.18 However, the kind of difficulties found in functioning of the moderately preterm children do conceptually match those of the very preterm children. This emphasizes the importance of the period of brain development between 32 and 37 weeks' gestational age. Although many (moderate) preterm children can survive, they cannot benefit from the neurobiological processes (eg, related to maternal thyroid hormone exchange19) during this period in the womb that may be specifically important for brain development and underlie the development of attention. Also, the formation of a mirror neurons system, possibly already present at birth,20 may be disturbed because of the different experiences in motor actions accompanying the changes in the immediate environment (womb or isolette). Hence, additional study of the development of all infants in the phase between 32 weeks' gestation until term age is necessary. Moderately preterm children should also be studied during infancy and at preschool age, because early signs of regulation and attention difficulties could be used to design focused intervention programs. In addition, studies are needed on parent-child interaction and the quality of the stimulation provided. Although it seems to have less serious consequences than very preterm birth, moderately preterm birth certainly needs additional attention.
We thank all the parents and children for their participation. The study was conducted in cooperation between Tilburg University, Elisabeth Hospital (J. Bruinenberg), Twee Steden Hospital (J. Bonenkamp) in Tilburg, Catharina Hospital (G. Couturier) in Eindhoven, St Anna Hospital (B. van den Boezem) in Geldrop, Elkerliek Hospital (E. Brouwer and N. Vaessens) in Helmond, Jeroen Bosch Hospital (C. Jacobs and L. Dekkers) in ′s Hertogenbosch, Oosterschelde Hospital (A. van der Hoop and J. Bauer) in Goes, and students Christina van Baalen, Eline Beeren, Anouk de Bruijn, Petra Cobussen, Karin Dekkers, Cathalijn Donders, Ilonka van den Heuvel, Petra deKnecht, Anita Rademakers, Elke van Rijsewijk, Kim Seerden, Yasemin Seref, Malou Smits, Marjolein Volaart, and Marijke deWit.
- Accepted November 6, 2008.
- Address correspondence to Anneloes L. van Baar, PhD, Utrecht University, Faculty of Social Sciences, PO Box 80140, 3508 TC, Utrecht, Netherlands. E-mail:
Financial Disclosure: The authors have indicated they have no financial relationships relevant to this article to disclose.
What's Known on This Subject:
Information on long-term development and functioning of moderately preterm children is scarce, despite the numbers of children involved (6% to 9% of all births) and their vulnerability resulting from their immature brain development at the time of birth.
What This Study Adds:
This study adds empirical data on school situation, cognitive performance, and socioemotional functioning assessed by mothers, fathers, and teachers, of moderately preterm children in comparison to term-born children at school age. The preterm group specifically shows attention difficulties.
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- ↵Achenbach TM, Rescorla LA. Manual for the ASEBA School-Age Forms & Profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families; 2001
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- ↵Central Institution of Statistics/Centraal Bureau voor de Statistiek. Basisonderwijs; leerlingen 2005/2006. Available at: http://statline.cbs.nl/StatWeb. Accessed May 14, 2008
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