Behavioral problems in very preterm children at five years of age using the Strengths and Difficulties Questionnaire: A multicenter cohort study

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Article

Reference

Behavioral problems in very preterm children at five years of age using the Strengths and Difficulties Questionnaire: A multicenter

cohort study

BARTAL, Timm, et al . & Swiss Neonatal Network and Follow-up Group

Abstract

Children born very preterm (VPT) are at increased risk of emotional and behavioral problems later in life. We aimed to determine the prevalence and spectrum of behavioral abnormalities at five years of age in VPT children.

BARTAL, Timm, et al . & Swiss Neonatal Network and Follow-up Group. Behavioral problems in very preterm children at five years of age using the Strengths and Difficulties Questionnaire: A multicenter cohort study. Early Human Development , 2020, vol. 151, p. 105200

DOI : 10.1016/j.earlhumdev.2020.105200 PMID : 33032050

Available at:

http://archive-ouverte.unige.ch/unige:155526

Disclaimer: layout of this document may differ from the published version.

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Contents lists available at ScienceDirect

Early Human Development

journal homepage: www.elsevier.com/locate/earlhumdev

Behavioral problems in very preterm children at five years of age using the Strengths and Difficulties Questionnaire: A multicenter cohort study

Timm Bartal

^a

, Mark Adams

^b

, Giancarlo Natalucci

^a,b

, Cristina Borradori-Tolsa

^c,1

, Beatrice Latal

^a,d,^⁎^,1

, the Swiss Neonatal Network and Follow-up Group

a Child Development Center, University Children's Hospital, Zurich, Switzerland

b Department of Neonatology, University of Zurich, Zurich University Hospital, Zurich, Switzerland

c Division of Development and Growth, Department of Child and Adolescent, University Hospital, Geneva, Switzerland

d Children's Research Center, University Children's Hospital, Zurich, Switzerland

A R T I C L E I N F O Keywords:

Behavior Early childhood Neurodevelopment Premature birth

A B S T R A C T

Introduction: Children born very preterm (VPT) are at increased risk of emotional and behavioral problems later in life. We aimed to determine the prevalence and spectrum of behavioral abnormalities at five years of age in VPT children.

Methods: Multi-center cohort study on 339 early-school aged children born at a gestational age below 32 weeks, between 2008 and 2011 and followed through the SwissNeoNet. Behavior was assessed with the Strength and Difficulties Questionnaire and compared to published German norms. Analysis of perinatal, neonatal, socio-eco- nomic and neurodevelopmental risk factors was performed using multivariable logistic regression.

Results: 30.7% of 1105 VPT surviving children were assessed at mean age 67.3 months (SD 5.9). Compared to the reference population, VPT children had significantly higher scores for emotional symptoms (odds ratio 1.53, 95% confidence interval 1.11.-2.12), while the total difficulties score was similar (1.16, 0.85–1.58). Lower socioeconomic status was the only independent predictor of at-risk behavior (borderline and abnormal behavior).

Conclusion: The spectrum of behavioral abnormalities in a current Swiss cohort of VPT children differs from the previously published data as hyperactivity was not a prominent symptom. Instead, emotional problems were reported to occur more frequently, with an increased prevalence for those coming from a lower socioeconomic background.

1. Introduction

Children born very preterm (VPT) are at increased risk of neurodevelopmental impairment [1,2]. In addition, behavioral problems remain a concern in the VPT population [3]. Several studies confirmed that premature birth is associated with an increased risk for the development of emotional and behavioral problems throughout infancy, at school-age and well into adolescence [1,4–6]. The number of studies investigating behavioral impairments in VPT children at preschool and school age increased considerably in the last decade, but they differ greatly in design and assessment tool.

The majority of studies reporting behavior in VPT mainly rely on information obtained through questionnaires [5,7–10]. The Strengths and Difficulties Questionnaire (SDQ) [5,11] is a short questionnaire widely used to screen for behavioral problems in children aged 4 to

16 years, which can be filled in by parents or teachers. Using the SDQ, the prevalence of behavioral problems ranges from 13 to 46% in VPT children. Behavioral problems in VPT may become evident already during preschool age. For school-age children, Johnson and Marlow described a “preterm behavioral phenotype”, which is characterize by inattention, anxiety, and social difficulties [12]. In contrast, the French population-based EPIPAGE study found higher difficulties scores on every behavioral scale of the SDQ at the age of five years [5].

Since the spectrum and prevalence of behavioral problems in VPT children remain open, this study aims to describe the behavioral problems and emotional competences at five years of age in a recent Swiss cohort of children born VPT. We hypothesize to find higher total diffi- culties scores in the SDQ assessment. As hyperactive and inattentive behavior seem to be more prevalent at the age of three to five years we also expect to find higher test scores in the hyperactivity subscale [13].

https://doi.org/10.1016/j.earlhumdev.2020.105200

Received 3 February 2020; Received in revised form 26 July 2020; Accepted 22 September 2020

⁎Corresponding author at: Child Development Center, University Children's Hospital, Steinwiesstrasse 75, CH - 8032 Zurich, Switzerland.

E-mail address: bea.latal@kispi.uzh.ch (B. Latal).

1Shared last authorship: both authors contributed equally to this paper.

Available online 23 September 2020

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Moreover, we aimed to examine risk factors associated with behavioral problems to help identify children in need of psychological intervention at an early stage.

2. Methods 2.1. Study population

In this retrospective multicenter cohort study, we included all children born between January 2008 and December 2011 and below 32 weeks of gestation. They were all included in the Swiss Neonatal Network & Follow-Up Group (SwissNeoNet). Data on behavior were retrieved from the following four Swiss tertiary care centers: Basel, Chur, Geneva and Zurich. SDQ questionnaire were distributed to all parents of children who were seen at the five- year follow up assessment. There were no exclusion criteria for questionnaire distribution.

Children that had available SDQ parental report and concluded the 5- year follow-up assessment (5-FU) by the time of data analysis (age at follow-up: mean 67.3 months (SD 5.9)) were eligible for data analysis.

2.2. Neonatal data

Neonatal data was extracted from the prospective national database of the Swiss Neonatal Network. Gestational age (GA), birth weight z- scores, major brain injury, bronchopulmonary dysplasia (BPD), retinopathy of prematurity, necrotizing enterocolitis, neonatal sepsis and Socio-economic status (SES) were defined as previously published for this cohort [3,14].

2.3. Instruments and measures

Behavior at the age of five years was rated by the parents using the SDQ [15] and the data was collected prospectively between 2013 and 2016. The parents were asked to complete the German or French parental report version.

The questionnaire is divided into five sections with five questions each, resulting in a total number of 25 questions. The five sections screen for emotional symptoms (e.g. Item 24: “Many fears, easily scared…”), conduct problems (e.g. Item 18: “Often lies or cheats”), hy- peractivity/inattention (e.g. Item 10: “Constantly fidgeting or squirming”), peer problems (e.g. Item 19: “Picked on or bullied by other children…”) and prosocial behavior (e.g. Item 4: “Shares readily with other children…”) [15]. Each item is scored on a three-point scale of 0 = not true, 1 = somewhat true and 2 = certainly true. The scores for each subscale are calculated by adding scores on items relevant to a particular problem. The SDQ also provides a total difficulties score (0–40 points) which is calculated by summing up all subscale scores (0–10 points) except prosocial behavior subscale, as this is the only domain where a higher score expresses positive behavior.

SES was evaluated at the time of birth and at the time of follow-up.

Since SES is important for subsequent early child development and behavior, the SES assessed at birth was used for analysis. The score ranges from 2 to 12 points and is based on the sum of the mother's educational level and the father's occupational level on a scale of 1–6 points each. A low score indicates high socio-economic status, whereas a high score indicates low status [16].

Intelligence (IQ) was assessed at 5-FU with the Kaufman Assessment Battery for Children (K-ABC) [17]. 23 children had missing IQ values due to missing subscores necessary to calculate a total IQ. Cerebral palsy (CP) was graded according to the Gross Motor Function Classifi- cation System (GMFCS) [18]. Attention-Deficit/Hyperactivity Disorder (ADHD) and Autism spectrum disorder were considered if the patient had a positive history of diagnosis by a pediatric specialist for it and/or had ongoing pharmacotherapy in case of ADHD. A history for or finding of severe visual or severe auditory problems and current physical or occupational therapy were also assessed.

2.4. Statistical analysis

Values used in this study are SDQ total difficulties score, total scores for each subscale and cut-off values for three bands normal, borderline Abbreviations

5-FU 5-year Follow-up group BPD Bronchopulmonary dysplasia GA Gestational age

K-ABC Kaufman Assessment Battery for Children LOS Late onset sepsis

SDQ Strengths and Difficulties Questionnaire SES Socio-economic status

VPT Very Preterm

1356 infants 22 0/7 - 31 6/7 weeks

born 2008-2011 four centers in Switzerland

339 (30.7% of survivors) with SDQ and 5-year follow-up 251 died

114 in delivery room

1105 (81.5%) surviving infants

471 (42.6% of survivors) without 5-year follow-up or SDQ

assessment

295 (26.7% of survivors) with 5- year follow-up but without SDQ

assessment

Fig. 1. Study flow sheet.

T. Bartal, et al. Early Human Development 151 (2020) 105200

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and abnormal. The three bands were categorized according to pre- viously published normative data of a German collective, since no SDQ data for Swiss term born children exists [19]. For risk factor analysis, we combined children in the borderline and abnormal group into an at- risk group, as we considered the borderline group to be at-risk and wanted to include all children at-risk for behavioral problems.

Difference analysis in baseline characteristics between children with and without SDQ data and the children with normal, borderline and abnormal (resp. normal and at-risk) SDQ total difficulties scores and subscores was performed using Chi-Square for nominal variables and t- test for independent samples for interval scaled variables. Risk factor analysis was performed using a multivariable logistic regression model.

Probability values below 0.05 were considered significant. Statistical analyses were performed using IBM SPSS Version 25 and Microsoft Excel Version 16.

Data collection and evaluation for this study were approved by the Swiss Federal Commission for Privacy Protection in Medical Research and the Zurich Ethics Committee (KEK-ZH-Nr2014-0552). Both parents and children were informed of the voluntary nature of data collection.

3. Results

3.1. Study population

Of 1356 children born alive before 32 weeks of gestation between 2008 and 2011, 1105 survived and were thus eligible for SDQ assessment and 5-FU. Of those, 471 (42.6% of survivors) neither participated in the 5-FU nor filled out the SDQ. Further, 295 (26.7%) participated in the 5-FU but did not take part in the SDQ survey. Consequently, 339 (30.7%) VPT born children had information on the SDQ and a 5-FU assessment (see Fig. 1). Mean age at follow-up was 67.3 months (SD 5.9).

Neonatal baseline characteristics were comparable between participants and non-participants except for a lower GA and a higher rate of BPD and late onset sepsis (LOS) in participants. SES was also higher in participants (lower score) (Table 1).

Of five children in our sample with a major birth defect one child had agenesis of the corpus callosum, two had an atrial septal defect, one had a ventricular septal defect and one had a combination of a patent foramen ovale, a small atrial septal defect and a small ventricular septal defect. The rate of major birth defects in the non-participants group was more than twice as high than in the participating group.

3.2. Behavioral outcome

Compared to term born children, VPT born children showed similar rates of normal, borderline and abnormal overall behavior (total difficulties score) than controls (see Table 2). “At risk behavior”, defined as the combination of borderline and abnormal behavior was found in 70 of VPT children (20.6%) and was similar to those in the term group (18.4%). Significantly higher rate of “at risk behavior” was found in the emotional symptoms, while the rate of abnormal prosocial behavior was lower in the VPT group. The combination of normal and borderline behavior in comparison to abnormal behavior showed similar rates. The corresponding rates are reported as odds ratios in two different col- umns.

3.3. Risk factor analyses

Only SES was associated with “at-risk behavior”. There was no association found between birth weight z-score, major brain injury (intraventricular hemorrhage ≥ Grade 3, periventricular leucomalacia), IQ < 85, neurodevelopmental morbidity (CP, severe visual or severe auditory problems, IQ < 85, epilepsy), behavioral morbidity (ADHD, Autism spectrum disorder) or current therapy (current physical or oc- cupational therapy) and “at-risk behavior” (see Table 3). The same

multivariable logistic regression model was repeated for all five sub- scales scores and no significant association was found for any of the previously mentioned markers to higher subscale scores.

4. Discussion

In this retrospective multicenter cohort study a higher prevalence of emotional symptoms and prosocial behavior at preschool age could be demonstrated for children born VPT. Surprisingly, overall behavioral abnormality and hyperactive/inattention symptoms were not significantly more prevalent in the VPT subjects than in the term born control group.

The SDQ has been proven to be an excellent tool for screening behavioral disorder and is one of the most frequently used questionnaires for screening behavioral health problems in children born prematurely.

Its popularity can be explained by its brevity and acceptability among parents [20]. A large British cohort showed that the SDQ had a high reliability and SDQ scores were highly correlated to other previously established diagnostic tools as the CBCL [21]. However, it is important to note that the prevalence of mental health problems is slightly over- estimated when only parental assessment is obtained, since single-informant (e.g. only completion by parents) is inferior to multi-informant (e.g. additionally assessed by teacher) assessment [20].

In our study, comparing to German norms, emotional problems occurred more frequently in VPT children. High prevalence for emotional symptoms were reported consistently by several other studies, whereas the rate for conduct problems was usually not elevated up until the age of five years [1,4,5,11]. Differences in socio-emotional behavior between VPT and term born children have been reported in infancy [22], childhood [23] and up to adolescence [24]. Importantly, VPT children with emotional problems at five years of age were more likely to be diagnosed with a psychiatric disorder at age seven years [25].

The similar prevalence of hyperactivity/inattention symptoms in our sample contradicts recent findings that demonstrate a significant difference in the hyperactivity domain between preterm born children and controls at five years of age [5]. As participating parents in our study had a significantly higher SES, the rate of behavioral problems, in particular hyperactivity, in VPT children may have been lower and thus Table 1

Comparison of baseline characteristics of study participants and non-participants.

Participants Non-

participants p-Value (n = 339) (n = 766)

Gestational age [weeks], mean (SD) 29.2 (1.8) 29.4 (2) 0.02 Birth weight z-score, mean (SD) −0.05 (0.76) −0.06 (0.81) 0.84

Female gender, n (%) 169 (49.9) 376 (49.1) 0.81

Male gender, n (%) 170 (50.1) 390 (50.9) 0.81

Antenatal corticosteroids

(completed), n (%) 249 (73.5) 534 (69.7) 0.30

Multiple, n (%) 132 (38.9) 279 (36.4) 0.43

Major birth defect, n (%) 5 (1.5) 26 (3.4) 0.07

Bronchopulmonary dysplasia, n (%) 42 (12.4) 59 (7.7) 0.008 Necrotizing enterocolitis, n (%) 5 (1.5) 2 (0.3) 0.55

Early onset sepsis, n (%) 7 (2.1) 10 (1.3) 0.35

Late onset sepsis, n (%) 45 (13.3) 62 (8.1) 0.008 ROP grade 3 or higher, n (%) 9 (2.7) 20 (2.6) 0.92 Major brain injury, n (%) 14 (4.1) 30 (3.9) 0.89 Length of stay^a[days], mean (SD) 62 (26) 60 (28) 0.40 Socioeconomic status^b, mean (SD) 5.6 (2.6) 6.1 (2.8) 0.01 ROP, retinopathy of prematurity.

a Length of stay until 1st discharge home.

b A low score indicates high socio-economic status. Range from 2 to 12 points: education level of mother on a scale 1–6 points plus occupational level of father on a scale 1–6 points, according to Largo et al. (see text for full reference).

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we may not have been able to find a difference between VPT and controls [26]. We also found a higher rate of prosocial behavior in the VPT children compared to the control population which may also result from a higher SES in the VPT group compared to the control group.

ADHD is the most prevalent psychiatric disorder reported in the preterm population [27]. The inattentive ADHD subtype seems to be more prevalent particularly in older VPT children than in term-born children. This increased risk for ADHD inattentive subtype may be related to global changes in brain anatomy and connectivity [6] often observed in this population. Also, in the clinical setting and in particular with younger children, the diagnosis of the inattentive ADHD type is often difficult as hyperactive symptoms are more easily reported by parents and teachers and inattention often only becomes relevant in the school setting. This may contribute to the low rate of reported ADHD diagnoses in our sample. The low prevalence of abnormal

hyperactivity/inattention scores in the SDQ is in line with this finding and raises the question whether the SDQ better captures hyperactivity symptoms than inattention symptoms. Therefore, VPT children sus- pected of having an ADHD should benefit from a more focused clinical assessment for attentional problems.

Even though the number of studies investigating behavioral disorders of preterm birth has steadily increased, research mostly focussed on children at school age and early adolescence. Only few studies in- vestigated behavioral problems at preschool age so far and thus in- consistency in results could also be attributed to cultural and institu- tional differences in perceiving and evoking behavioral vulnerabilities between countries [13].

Our sample includes VPT children with a higher prevalence of BPD and LOS and a younger gestational age. These medical risk factors may constitute a higher risk for adverse long term outcome [14]. However, we did not find a negative effect on behavioral outcome at five years of age.

As mentioned above, the level of parental education and occupation in this sample was high. Since higher SES may be associated with an increased parental awareness and concerns regarding the development of their child, parents of VPT children with a higher SES may have been more willing to participate in this study. Since SES is a strong de- terminant of child development [28], the high mean SES in the evaluated sample of VPT children may have led to an underestimation of the prevalence of behavioral difficulties in the source population.

Despite this selection bias, there was evidence that low SES was associated with higher SDQ total difficulties score. This implies that the postnatal environment has a higher impact on behavioral outcome than neonatal morbidity. Aside from environmental and maturational factors, there is evidence that cerebral alterations can lead to behavioral difficulties in VPT children. Several neuroimaging studies support this link. Specifically, behavioral problems were related to alterations of the orbitofrontal cortex [24,29], which is considered particularly vulnerable in premature infants [30]. Interestingly, in our study, con- sequences of altered brain development such as neurodevelopmental impairments (e.g. CP, low IQ) or psychiatric disorders (ADHD, Autism Table 2

Behavioral outcome stratified by SDQ category.

Preterm group Term group [1] OR (95% CI) OR (95% CI)

n (%) (n = 339) (n = 930) Reporting OR for being in any other than the normal group Reporting OR for being in the abnormal group

Total difficulties 1.16 (0.85–1.58) 0.97 (0.64–1.47)

Normal 269 (79.4) 759 (81.6)

Borderline 37 (10.9) 78 (8.4)

Abnormal 33 (9.7) 93 (10)

Emotional symptoms 1.53 (1.11–2.12)^⁎ 1.73 (1.16–2.59)^⁎

Normal 271 (79.9) 800 (86)

Borderline 25 (7.4) 59 (6.3)

Abnormal 43 (12.7) 72 (7.7)

Conduct problems 0.81 (0.56–1.16) 0.94 (0.56–1.57)

Normal 296 (87.3) 788 (84.7)

Borderline 22 (6.5) 81 (8.7)

Abnormal 21 (6.2) 61 (6.6)

Hyperactivity/inattention 1.10 (0.78–1.55) 1.03 (0.68–1.56)

Normal 285 (84.1) 793 (85.3)

Borderline 20 (5.9) 46 (4.9)

Abnormal 34 (10.0) 91 (9.8)

Peer problems 0.80 (0.54–1.18) 0.66 (0.38–1.16)

Normal 302 (89.1) 806 (86.7)

Borderline 21 (6.2) 59 (6.3)

Abnormal 16 (4.7) 65 (7)

Prosocial behavior 0.43 (0.28–0.67)^⁎ 0.36 (0.18–0.72)^⁎

Normal 314 (92.6) 785 (84.4)

Borderline 16 (4.7) 79 (8.5)

Abnormal 9 (2.7) 66 (7.1)

[1] Woerner W, Becker A, Friedrich C, et al. Normierung und Evaluation der deutschen Elternversion des Strengths and Difficulties Questionnaire (SDQ): Ergebnisse einer repräsentativen Felderhebung. Zeitschrift für Kinder- und Jugendpsychiatrie und Psychotherapie 2002; 30: 105–112.

⁎ p < 0.01.

Table 3

Association of medical characteristics with at-risk^#behavior (multivariable logistic regression model).

Mean (SD), N (%) OR (95% CI) Gestational age [weeks], mean (SD) 28.70 (1.84) 0.95 (0.79–1.14) Birth weight z-score, mean (SD) −0.11 (0.84) 0.81 (0.53–1.24)

Major brain injury^a, n (%) 1 (0.3) 0 (0)

IQ^b< 85, n (%) 12 (3.5) 3.41 (0.35–33.38)

Socio-economic status, mean (SD) 6.36 (2.67) 1.14 (1.00–1.29)^⁎ Neurodevelopmental morbidity^c, n (%) 14 (4.1) 0.36 (0.04–3.29) Psychiatric disorders^d, n (%) 6 (1.8) 2.17 (0.50–9.49) Current therapy^e, n (%) 10 (2.9) 1.42 (0.53–3.77)

# Composite of borderline (n = 26) and abnormal SDQ (n = 28) test scores.

⁎ Significant, p < 0.05.

a Intraventricular hemorrhage ≥ Grade 3 or periventricular leucomalacia.

b K-ABC (SIF), K-ABC II (FKI).

c Cerebral Palsy, severe visual or severe auditory problems, IQ < 85, Epilepsy.

dADHD (n = 2), Autism spectrum disorder (n = 2).

e Current physical or occupational therapy.

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spectrum disorder) were not associated with SDQ measures. Since the absolute number of these conditions was small, the power to detect such an association may have been too weak.

The present study has limitations worth mentioning. Reference values for term born controls were used from a previously published sample of children born in Germany [19] as norms for Swiss children are not available. In addition, the German norms by Woerner et al. [19]

included children aged six to sixteen years while the mean age in our sample was five years (66.5 months). It is conceivable that the comparison of our data to a reference sample of five-year old healthy children would have altered the results. Since Woerner et al. did not report any raw baseline characteristics, the term born control group could not be described sufficiently. We therefore were unable to adjust for differences in baseline characteristics. This would be important to appropriately interpret the pattern of our results. In addition, we did not have teacher's perspective as in some regions, children enter kin- dergarten after five years of age. Furthermore, the rate of children with a 5-FU and SDQ assessment among survivors was rather small and may have introduced a parental reporting bias.

5. Conclusion

This study adds important evidence for the understanding of the behavioral phenotype of children born VPT in Switzerland. Parents reported higher rates of emotional problems. In addition to current research our study adds to the evidence that VPT are indeed vulnerable to behavioral disorders. Additionally, it appears that the neonatal period has less impact on behavior than environmental factors. This emphasizes the importance of the postnatal period as a protective factor against the development of behavioral disorders. To better understand the specific aspects of environmental factors that contribute to this effect, further research has to be conducted.

Declaration of competing interest/financial disclosure

Mark Adams receives a salary as network coordinator for the Swiss Neonatal Network. Giancarlo Natalucci received financial support by the Swiss National Science Foundation; grant PZOOP3_161146. The remaining authors have indicated they have no potential conflicts of interest relevant to this article to disclose.

CRediT authorship contribution statement

Timm Bartal: Data curation, Formal analysis, Visualization, Writing - original draft, Writing - review & editing. Mark Adams:

Conceptualization, Methodology, Data curation, Formal analysis, Writing - review & editing. Giancarlo Natalucci: Conceptualization, Investigation, Methodology, Supervision, Validation, Writing - review &

editing. Cristina Borradori-Tolsa: Investigation, Methodology, Supervision, Validation, Writing - review & editing. Beatrice Latal:

Conceptualization, Investigation, Methodology, Supervision, Validation, Writing - review & editing.

Acknowledgements

We thank the Swiss Neonatal Network and Follow-up Group (SwissNeoNet) member hospitals that contributed data used in this study.

Basel: University of Basel Children's Hospital (UKBB), Department of Neonatology (S. Schulzke), Department of Neuropediatric and Developmental Medicine (P. Weber); Chur: Children's Hospital Chur, Department of Neonatology (T. Riedel), Department of Neuropediatric (E. Keller, Ch. Killer); Geneva: Department of Child and Adolescent, University Hospital (HUG), Neonatology Units (R. E. Pfister), Division of Development and Growth (P. S. Huppi, C. Borradori-Tolsa); Zurich:

University Hospital Zurich (USZ), Department of Neonatology (D.

Bassler, R. Arlettaz), University Children's Hospital Zurich, Department of Neonatology (C. Hagmann), and Child Development Centre (B. Latal, G. Natalucci), Hospital Zollikerberg (V. Bernet).

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