A longitudinal perspective on behavioral outcomes of preterm children: looking beyond composite scales

Introduction: This study aimed to evaluate parental perspectives on behavioral development in preterm children over time, and to evaluate the impact of adverse early life events on multiple domains of behavior.

Methods: Single-center cohort study (January 2010 – December 2016) including children born between 24 and 30 weeks' gestation. Behavior was investigated using the Child Behavior Checklist (CBCL) at 2, 5.5 and 8 years' corrected age. As a proxy of adverse early life events, we used a binary composite measure indicating the presence of any of the following: postnatal corticosteroid administration, perinatal brain injury, surgical interventions or prolonged ventilation. Linear mixed model analysis was used to explore behavioral development over time and associations with adverse early life events.

Results: In total, 204 children had CBCL assessments at all ages. Attention problems (20%) and anxious-depressed (13%) behavior showed the highest clinically relevant scores and steepest increase over time, respectively. Exposure to adverse early life events was associated with attention problems and withdrawn behaviors.

Discussion: Subscale-level evaluation characterizes the behavioral phenotype of preterm children and shows a progressive increase in difficulties over time. Exposure to adverse early life events is associated with increased problems across multiple behavioral domains. Identifying at-risk children may facilitate accurate monitoring and targeted intervention.

1 Introduction

Preterm birth is associated with a variety of adverse long-term outcomes, including behavioral difficulties that persist throughout childhood (Allotey et al., 2018; Arpi and Ferrari, 2013; Delobel-Ayoub et al., 2009; Hornman et al., 2016). These difficulties often manifest as limited attention, hyperactivity, lower adaptive abilities, and impaired social skills (Aarnoudse-Moens et al., 2009; Arpi and Ferrari, 2013; Delobel-Ayoub et al., 2009). Over the past decades, behavioral outcomes of preterm children have not improved (Larsen et al., 2024). Recent review articles confirm that preterm children – especially those born before 32 weeks of gestation – are at increased risk for persisting attention deficits (Jaeger et al., 2025; Kollndorfer et al., 2025). This highlights the need for a deeper understanding of the mechanisms underlying these difficulties.

The behavioral patterns observed in preterm children can be interpreted within the framework of the preterm behavioral phenotype. This framework describes a set of commonly co-occurring symptoms – including attention problems, anxiety and social difficulties – which have been linked to brain development following preterm birth (Fitzallen et al., 2020; Palanivel et al., 2025). As such, the preterm behavioral phenotype framework offers a valuable perspective for understanding behavioral trajectories of preterm children (Palanivel et al., 2025).

Previous research has predominately concentrated on composite behavior outcome measures, such as internalizing and externalizing behavior (Aarnoudse-Moens et al., 2009; Allotey et al., 2018; Hornman et al., 2016). Although some studies have explored behavioral difficulties across multiple domains, they have typically done so at a single time point, focused on a specific behavioral subdomain, limited their scope to the preschool period, or initiated assessments later in childhood (Arpi and Ferrari, 2013; Delobel-Ayoub et al., 2009; Linsell et al., 2019). Given the persistence of behavioral difficulties throughout childhood and the dynamic trajectories of neurobehavioral development in preterm born children (Hornman et al., 2016), adopting a longitudinal and domain-specific perspective is essential for understanding these outcomes.

Since behavioral development consists of a complex interplay of factors, it should be understood within a broader context (Aarnoudse-Moens et al., 2009; Arpi and Ferrari, 2013; Delobel-Ayoub et al., 2009). For preterm born children, this context involves both perinatal characteristics and environmental factors. Lower gestational age (GA) at birth, exposure to pain and stress during neonatal hospitalization, and the presence of neonatal morbidities have been linked to increased behavioral difficulties later in childhood (Goncalves et al., 2025; Valeri et al., 2015). Environmental factors such as maternal age, education and wellbeing, and family income also play an important role in shaping the behavioral outcomes of preterm children (Delobel-Ayoub et al., 2009; Flouri et al., 2014; Peralta-Carcelen et al., 2017).

Although adverse early-life circumstances are well-documented to affect preterm children and their families, the persistence of these effects and their influence on behavioral development over time remain insufficiently understood. Therefore, the aim of this study was to explore parent-reported behavioral outcomes of preterm children across childhood and to investigate the impact of adverse early life events on behavioral development across multiple domains, from infancy through school age.

2 Materials and methods

2.1 Patient population

Preterm children born between 24 and 30 weeks' gestation or with a birth weight (BW) below 1000g, inborn or admitted to the neonatal intensive care unit (NICU) of Máxima MC within 24h after birth between January 2010 and December 2016 and with ≥1 follow-up assessment at 2, 5.5 or 8 years were eligible for inclusion in this study. Children of parents living outside of the adherence area of Máxima MC, post-partum referrals from other hospitals and children with major congenital malformations were excluded. The ethical review board of Máxima MC approved the study and waived informed parental consent (N17.166).

2.2 Perinatal data

Perinatal data are collected from electronic patient files. This includes the following perinatal information: GA (weeks), birth weight (BW; grams), small for gestational age (SGA; defined as birth weight below the 10^th percentile according to Hoftiezer growth charts (Hoftiezer et al., 2019), yes or no), Apgar score at 5 min postpartum (Apgar, 1953), treatment with antenatal corticosteroids (none, incomplete course; defined as one or two doses of betamethasone of which the second dose was administered < 24 h before birth, and complete course; defined as two doses of betamethasone of which the second dose was administered >24 h before birth), and administration of postnatal corticosteroids for weaning off the ventilator (yes or no). It also includes clinical information on perinatal brain injury (defined by serial ultrasound imaging as intraventricular hemorrhage (IVH) grade III-IV or white matter injury (de Vries et al., 1992; Papile et al., 1978), yes or no), early onset sepsis (positive blood culture ≤ 72 h after birth, yes or no), late onset sepsis (positive blood culture taken >72 h after birth, yes or no), and information on interventions including laparotomy for necrotizing enterocolitis (NEC) or intestinal perforation (yes or no), ductal ligation (yes or no), primary laser treatment for retinopathy of prematurity (ROP) (yes or no), and ventilation during NICU admission (number of days). As a proxy for adverse early life events, a binary composite outcome measure (yes or no) was used, indicating the presence of any of the following during NICU admission: postnatal corticosteroid administration, perinatal brain injury, laparotomy, ductal ligation, or ≥14 days of ventilation, as previously described.

2.3 Follow-up

After NICU admission, patients are invited for follow-up visits to the outpatient clinic of Máxima MC, in line with the Dutch national perinatal follow-up guidelines (Rijken, 2015). In this standardized follow-up program, all children born before 30 weeks' GA and/or with BW below 1000 g are invited for follow-up visits at the corrected ages of 2, 5.5 and 8 years. During these visits, children are assessed by a trained team of neonatologists, physical therapists and developmental psychologists.

2.4 Behavioral outcomes

At 2, 5.5 and 8 years, behavioral development is assessed using the parent-report Child Behavior Checklist (CBCL) questionnaire (Achenbach, 1999). This questionnaire is designed and validated for behavioral assessment of children aged 1.5 to 18 years and is part of the Dutch national neonatal follow-up guideline (Nederlands Jeugdinstituut, n.d.; Rijken, 2015). Two CBCL versions exist, which are tailored to the age of the child: the CBCL/1.5–5 for children up to preschool age, and the CBCL/6–18 for school-aged children and adolescents (Nederlands Jeugdinstituut, n.d.). In addition to the total behavioral problems scale and the composite scales of internalizing and externalizing behaviors, the CBCL provides information about multiple subscales of behavior. The CBCL/1.5–5 includes seven subscales: emotionally reactive, anxious/depressed, somatic complaints, withdrawn, sleep problems, attention problems and aggressive behavior (Nederlands Jeugdinstituut, n.d.). The CBCL/6–18 contains eight subscales: anxious/depressed, withdrawn/depressed, somatic complaints, social problems, thought problems, attention problems, rule-breaking behavior and aggressive behavior (Nederlands Jeugdinstituut, n.d.). Scores are transformed into norm-referenced standard or t-scores which have a mean of 50 and standard deviation (SD) of 10 in the general population, and take gender and age differences into account (Guerrera et al., 2019). Higher scores indicate more parent-perceived behavioral problems (Guerrera et al., 2019). A t-score of 60 (>1 SD) or above is generally considered clinically relevant, with t-scores ≥65 indicating clinically present symptoms (Guerrera et al., 2019).

2.5 Statistical analysis

Differences in baseline characteristics between children with complete (i.e., follow-up at age 2, 5.5 and 8), incomplete (i.e., follow-up at 1 or 2 time points) and no follow-up were assessed using chi-square tests for categorical variables and univariate ANOVA for continuous variables. To adjust for multiple testing, Bonferroni corrections were applied to between-group comparisons. Consequently, baseline differences between groups were considered statistically significant if p < 0.017. In case of a significant result, post-hoc pairwise comparisons were used to pinpoint the specific groups that differed. To explore CBCL scores and differences from the normative mean scores, descriptive statistics and one-sample t-tests were used. To explore behavioral development over time and the impact of adverse early life events on behavioral outcomes, linear mixed models were used for all CBCL subscales that were measured at a minimum of 2 time points. The models included a fixed effect of time and of adverse early life events as previously defined. The interaction term of these two fixed effects was also included. To account for individual variation, a random intercept was added to the models. In the mixed model analysis, a p-value below 0.05 was considered statistically significant. Corrections for multiple testing were not applied to the mixed models, since each model explored an individual hypothesis per behavioral domain (Rubin, 2021). To explore potential non-independence due to multiple children from the same household, we performed an exploratory sensitivity analysis randomly retaining only one child per household. To complete baseline characteristics, missing values for perinatal characteristics (Apgar score n = 1, antenatal corticosteroid administration n = 7, maternal education level n = 48) were imputed through single imputation in the “mice” package in R version 4.4 using all baseline participant characteristics and CBCL scores. No imputed variables were used in the linear mixed model analysis. All descriptive and mixed modeling analyses were done using IBM SPSS Statistics version 29.

3 Results

3.1 Participant characteristics

A total of 478 children were born during the inclusion period. Of these, 71 (15%) died and 7 (1%) were excluded due to congenital malformations, resulting in 400 children being eligible for inclusion in the current study (Figure 1). Of those, 204 (51%) had CBCL follow-up assessments at ages 2, 5.5, and 8, 145 (36%) had at least one CBCL follow-up assessment and 51 (13%) had no follow-up assessments. Characteristics of children with complete, incomplete and no follow-up information are presented in Table 1. We observed a significantly higher proportion of laparotomy procedures among children without follow-up compared to those with incomplete and complete follow-up (p < 0.001). This discrepancy is attributable to the fact that neonatal surgeries are not performed at our hospital; consequently these children were transferred elsewhere for treatment and were not enrolled in our follow-up program. Additionally, maternal education level was lower in children without complete follow-up (p < 0.001).

Figure 1

Figure 1. Flow diagram of participant inclusion. BW, birth weight; CBCL, child behavior checklist; GA, gestational age; NICU, neonatal intensive care unit.

Table 1

Table 1. Baseline characteristics of children with and without complete CBCL follow-up assessments at 2, 5.5 and 8 years of age.

3.2 CBCL scores

In general, total behavioral scores and composite internalizing and externalizing scores did not differ significantly from the normative mean at ages 2, 5.5, and 8 (Table 2). The subscale scores are presented in Table 3. Scores on nearly all CBCL subscales increased over time, accompanied by a progressive increase in the proportion of children with clinically relevant scores at every assessment. T-scores ≥65 in the domains of attention problems (20%) and anxious-depressed behaviors (13%) showed the highest scores and steepest increase over time, respectively. Figure 2 illustrates longitudinal trajectories of attention and anxious/depressed behavior scores across three developmental stages (ages 2, 5, and 8 years), combining stacked bar charts with (Sankey-style) flows to illustrate both cross-sectional distributions and individual transitions. Overall, developmental trajectories showed greater variability between ages 2 and 5 than between ages 5 and 8. Supplementary File 1 presents the longitudinal trajectories of all CBCL (subscale) scores across ages 2, 5.5, and 8.

Table 2

Table 2. CBCL composite scores of the included children.

Table 3

Table 3. CBCL subscale scores of the included children at 2, 5.5, and 8 years.

Figure 2

Figure 2. CBCL subscale scores of children with complete follow-up over time. The figure displays CBCL scores of 204 children (y-axis) with complete follow-up information. It shows how trajectories of behavior change from age 2 to 8 (x-axis).

3.3 Mixed model analysis

As shown in Table 4, linear mixed model analyses revealed that the overall fixed effect of time was statistically significant for 5/7 CBCL subscales, all indicating an increase in scores over time. Of these subscales, significant increases at 5.5 and 8 years compared to 2 years were observed for anxious-depressed (B_5.5 [95% CI] = 1 [0; 2]; B₈ [95% CI] = 3 [2; 4]), somatic complaints (B_5.5 [95% CI] = 1 [0; 2]; B₈ [95% CI] = 2 [1; 3]), attention problems (B₈ [95% CI] = 3 [2; 4]), and withdrawn behaviors (B_5.5 [95% CI] = 2 [1; 3]). While the overall effect of time was significant for the emotionally reactive subscale (F_{(1, 298)} = 9.08, p = 0.003), the parameter estimate comparing scores at 5.5 to those at 2 years was not statistically significant (B_5.5 [95% CI] = 1 [−1; 2]). In addition to the effect of time, having experienced adverse early life events was associated with significantly higher scores on attention problems (B [95% CI] = 2 [0; 4]) and withdrawn behaviors (B [95% CI] = 2 [1; 4]). Although the overall effect of adverse early life events was significant (F_{(1, 328)} = 6.75, p = 0.01) for emotionally reactive behavior, the parameter estimate indicated a non-significant increase (B [95% CI] = 1 [−1; 2]). The interaction effect between time and adverse early life events was significant for aggressive behavior only (F_{(2, 414)} = 3.52, p = 0.03). However, parameter estimates at 5.5 years (B [95% CI] = 1 [−1; 2]) and 8 years (B [95% CI] = −2 [−4; 0]) were not statistically significant, indicating that individual time-point contrasts should be interpreted with caution. Results from the sensitivity analysis excluding siblings yielded nearly identical outcomes for key subscales (anxious/depressed, attention problems and withdrawn behaviors), supporting the robustness of the primary findings.

Table 4

Table 4. Linear mixed model of time and adverse early life events.

4 Discussion

Subscale-level evaluations provide a valuable framework for exploration of behavioral trajectories of preterm children over time, offering a more nuanced characterization of the preterm behavioral phenotype. We observed a progressive increase in problems across nearly all behavioral domains from infancy through school age. Clinically present problems were most frequently observed in the domains of attention problems (20%) and anxious-depressed behaviors (13%), with the latter showing the steepest increase over time. Beyond the effect of time, exposure to adverse early life events was associated with poorer behavioral development in the domains of attention problems and withdrawn behaviors.

Our finding that preterm children experience more behavioral problems compared to the general population is in line with previous studies (Aarnoudse-Moens et al., 2009; Allotey et al., 2018; Arpi and Ferrari, 2013; Delobel-Ayoub et al., 2009; Linsell et al., 2019). However, this longitudinal study also found that behavioral problems significantly increase over time. T-scores ≥65 are indicative of clinically present symptoms (Guerrera et al., 2019), suggesting that preterm children present a range of behavioral challenges at school age. In our sample, the most prominent problems were observed in the domains of attention problems, anxious-depressed mood, and withdrawn behavior. This aligns with previous reports on the preterm behavioral phenotype, which describes a profile of co-occurring emotional, attentional, and social difficulties frequently observed in children born preterm (Burnett et al., 2019; Fitzallen et al., 2020; Palanivel et al., 2025).

Early behavioral problems have been shown to predict persistent or increased difficulties later in childhood (Hudziak et al., 2004). We observed that the proportion of children in the subclinical and clinical ranges increases progressively with age, particularly by 8 years, suggesting that a subset of children experience emerging or persistent problems over time (Figure 2). The connecting flows between assessments reveal patterns of stability and change, with most children remaining in the same category but some transitioning from normal to higher-risk classifications. A considerable proportion of children who demonstrated difficulties at age 8 had already exhibited such challenges at age 5, indicating a relative stability of behavioral problems within a subset of preterm children. Consistent with this finding, a previous study observed that 41% of very preterm children presenting behavioral problems at age 5 had already exhibited elevated difficulty scores at age 3, while 46% of those with behavioral difficulties at age 3 continued to experience such problems at age 5 (Delobel-Ayoub et al., 2009). Our findings support the dynamic nature of behavioral development and underscore the importance of early identification and targeted interventions to prevent escalation of difficulties during middle childhood.

Notably, CBCL scores may provide an underestimation of the severity of behavioral difficulties that the child is experiencing in daily life, as parents may be inclined to underreport the severity of behavioral difficulties of their child (Silva et al., 2024). Underreporting has been associated with parental mental health, social desirability bias, and limited parental awareness of their child's behavior in situations where parents are not present (Poulain et al., 2020; Silva et al., 2024). In line with this, lowering the CBCL t-score threshold for clinical relevance from 60 to 55 has previously been suggested (Hudziak et al., 2004).

As a proxy of adverse early life events, we employed a composite binary outcome measure indicating the presence of any of the following neonatal stressors: postnatal corticosteroid administration, perinatal brain injury, laparotomy, ductal ligation or prolonged ventilation). We found that exposure to such events negatively impacted attention and withdrawn behaviors. This finding aligns with previous research indicating that behavioral difficulties are associated with both preterm birth and exposure to adverse early life events (Goncalves et al., 2025; Valeri et al., 2015). A previous Dutch study reported that adolescents born very preterm showed fewer internalizing and attention problems compared to those born very preterm and a BW < 1,000 g (Hollanders et al., 2019). Similarly, a European study reported that increased GA and BW are associated with decreased internalizing, externalizing and attention problems and that these associations weaken or inverse in adolescence (Goncalves et al., 2025). Beyond GA and BW, other adverse early life events have been associated with later developmental outcomes of preterm children. For instance, exposure to painful neonatal procedures have been linked to altered behavioral trajectories, while medical complications have been shown to contribute to distinct neurodevelopmental outcome profiles in person-centered research (Momany et al., 2023; Valeri et al., 2015). Additionally, exposure to adverse childhood events has been associated with increased symptoms of attention deficit-hyperactivity disorder in children born very preterm (i.e., GA below 32 weeks), independent of socioeconomic factors (Bishop et al., 2025).

Our finding that a set of adverse early life events is associated with attention problems, difficulties in anxious and depressed emotions, and withdrawn behaviors aligns with previous reports. In addition to the well-reported attentional difficulties, previous research has found that preterm children with an extremely low birth weight possess poor social-emotional skills compared to other BW groups (Nagy and Kenyhercz, 2021). Potential mechanisms underlying attention problems and emotional dysregulation following early life adversity include disrupted brain maturation, altered stress physiology, and impaired caregiver-infant attunement. Adverse early life events may interfere with the development of neural circuits involved in executive functioning and emotion regulation – particularly in the prefrontal cortex, amygdala, and limbic system – leading to heightened emotional reactivity and reduced regulatory and attentional control (Smith and Pollak, 2020). Dysregulation of the hypothalamic-pituitary-adrenal axis may further contribute to persistent stress sensitivity, and difficulties modulating emotional responses (Niu et al., 2025). Finally, disruptions in caregiver-infant attunement may compromise the development of adaptive emotional and stress regulation capacities. Extremely low birth weight preterm children frequently show diminished adaptive functioning, particularly in self-care domains, and these difficulties may be influenced by parental overprotectiveness (Nagy and Kenyhercz, 2021). Additionally, parents' perspectives on their child's development are shaped by their own and their family's coping strategies, and the belief that developmental problems are temporary (Press Callahan et al., 2025). Preterm infants are more strongly impacted by the external factors mentioned above compared to their term-born peers (Cheong et al., 2020).

Identifying at-risk preterm children based on early life characteristics, as outlined in this study, is essential. As noted by Goncalves et al. (2025), such early identification may open “windows of opportunity for novel strategies, such as monitoring behavior” and facilitate targeted interventions to support neurodevelopmental outcomes (Goncalves et al., 2025). Alongside this, providing parents with adequate tools to help support their child's development is crucial. Effective communication between physicians and parents, combined with strategies to support parental coping strategies is key. Parents of extremely preterm children admitted to NICU vary in their emotional needs regarding support from nursing staff, social workers and psychologists (Bry and Wigert, 2019), emphasizing the need for tailored approaches. Consequently, future studies are needed to identify optimal and tailored strategies to provide parents with the support they need.

4.1 Strengths and limitations

The large sample size and longitudinal approach are notable strengths. To the best of our knowledge, this is the first study to investigate parental perspectives on behavioral development of preterm children across multiple time points up to school age. Importantly, we utilized all available subscales of behavior instead of focusing only on the composite scales of internalizing and externalizing behaviors. The refinement provided by incorporating the subscales can help to identify relevant mechanisms of behavioral development, especially given the predictive value of early behavioral problems. Identification of such mechanisms is needed for optimal monitoring and tailored developmental support. Moreover, our incorporation of mixed models to assess the impact of adverse early life events on parental perceptions of behavior may help to identify those preterm children who are particularly at risk for suboptimal behavioral development later in life.

Limitations include the single-center design, which may limit generalizability. CBCL assessments at all ages were available in 51% of the included children, indicating potential selection bias. CBCL reflects parental perspectives and may not be an objective measure of behavioral development. However, identification of psychosocial problems and subsequent action were 3–16 times more likely in children with clinical parent-reported problem behavior (Klein Velderman et al., 2010). This indicates that parents are well able to identify suboptimal development of their child. While the sensitivity analysis excluding siblings showed consistent results, the possibility of non-independence due to shared familial and/or environmental factors remains a limitation. Missing data for antenatal corticosteroid administration and Apgar scores was minimal, making single imputation appropriate, whereas its suitability for maternal education level was limited due to a higher amount of missing data. However, this is likely to have had little impact, as imputed variables were only used for descriptive baseline comparisons and excluded from subsequent analyses.

Lastly, we utilized a pragmatic approach of characterizing adverse early life events, based on the severity or complexity of complications during NICU stay, reflecting exposure to painful or stressful procedures. Future research could incorporate environmental factors into similar analyses to more comprehensively address the complex interplay shaping behavioral development over time.

4.2 Conclusions

Subscale-level evaluation characterizes the behavioral phenotype of preterm children and show a progressive increase in behavioral difficulties that may interfere with daily functioning by school age. Also, exposure to adverse early life events is associated with increased behavioral problems. The reported problems increase over time across nearly all subscales of behavior. Attention problems and anxious-depressed behavior show the highest prevalence and steepest increase over time, respectively. Attention-related problems are among the behavioral domains most significantly impacted by exposure to adverse early life events during the NICU period. Early identification of at-risk children may facilitate developmental monitoring and enable the implementation of targeted intervention. These strategies can be further strengthened by incorporating environmental factors, such as parenting practices and coping mechanisms, to optimally support the behavioral development of preterm children.

Data availability statement

The data analyzed in this study is subject to the following licenses/restrictions: The dataset used for this study is not publicly available due to patient privacy reasons. Requests to access these datasets should be directed to anVsaWEubWVpamVyQG1tYw==.

Ethics statement

The studies involving humans were approved by Ethical Review Board of Máxima MC. The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent for participation was not required from the participants or the participants' legal guardians/next of kin in accordance with the national legislation and institutional requirements.

Author contributions

JM: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing. SL: Data curation, Writing – review & editing. BV: Conceptualization, Writing – review & editing. PV: Conceptualization, Methodology, Supervision, Writing – review & editing. CV: Writing – review & editing. PA: Conceptualization, Data curation, Funding acquisition, Methodology, Supervision, Writing – review & editing.

Funding

The author(s) declared that financial support was received for this work and/or its publication. This project has been funded by a grant from Stichting Tiny & Anny van Doorne Fonds. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

The author(s) declared that this work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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The author(s) declared that generative AI was not used in the creation of this manuscript.

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Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fdpys.2025.1705552/full#supplementary-material

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