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Isolated CHDs and neurodevelopmental follow-up using the Bayley Scales of Infant and Toddler Development and the Ages and Stages Questionnaire at 18 and 36 months

Published online by Cambridge University Press:  11 June 2021

Mette Marie Baunsgaard*
Affiliation:
Institute for Clinical Medicine, Aarhus University, Aarhus, Denmark Department of Pediatrics and Adolescent Medicine, Aarhus University Hospital, Aarhus, Denmark
Tine B. Henriksen
Affiliation:
Institute for Clinical Medicine, Aarhus University, Aarhus, Denmark Department of Pediatrics and Adolescent Medicine, Aarhus University Hospital, Aarhus, Denmark
Charlotte K. Gilberg
Affiliation:
Department of Physio- and Occupational Therapy, Aarhus University Hospital, Aarhus, Denmark
Dorthe B. Wibroe
Affiliation:
Department of Physio- and Occupational Therapy, Aarhus University Hospital, Aarhus, Denmark
Trine Haugsted
Affiliation:
Department of Physio- and Occupational Therapy, Aarhus University Hospital, Aarhus, Denmark
John R. Østergaard
Affiliation:
Institute for Clinical Medicine, Aarhus University, Aarhus, Denmark Department of Pediatrics and Adolescent Medicine, Aarhus University Hospital, Aarhus, Denmark
Vibeke E. Hjortdal
Affiliation:
Institute for Clinical Medicine, Aarhus University, Aarhus, Denmark Department of Cardiothoracic Surgery, Rigshospitalet, Copenhagen, Denmark
Mette H. Lauridsen
Affiliation:
Institute for Clinical Medicine, Aarhus University, Aarhus, Denmark Department of Pediatrics and Adolescent Medicine, Aarhus University Hospital, Aarhus, Denmark
*
Author for correspondence: Mette Marie Baunsgaard, MS, Aarhus University & Department of Pediatrics and Adolescent Medicine, Aarhus University Hospital, Palle Juul Jensens Boulevard 99, Aarhus N 8200 Denmark. Tel: +45 26989281. E-mail: metbau@rm.dk
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Abstract

Objectives:

To compare early neurocognitive development in children born with and without isolated CHD using the Bayley Scales of Infant and Toddler Development (3rd edition) and the Ages and Stages Questionnaire (3rd edition).

Methods:

Recruitment took place before birth. Women expecting fetuses with and without CHD causing disturbances in the flow of oxygenated blood to the fetal brain were included in a prospective cohort study comprising fetal MRI (previously published) and neurodevelopmental follow-up. We now present the 18- and 36-month neurodevelopmental follow-up using the Bayley Scales according to age and the 6-month-above-age Ages and Stages Questionnaire in 15 children with and 27 children without CHD.

Results:

Children with CHD had, compared with the children without CHD, an increased risk of scoring ≤ 100 in the Bayley Scales cognition category at 18 and 36 -months; relative risk 1.7 (95% confidence interval (CI): 1.0–2.8) and 3.1 (CI: 1.2–7.5), respectively. They also achieved lower scores in the 6-month-above-age Ages and Stages Questionnaires (24 and 42 months) communication; mean z-score difference −0.72 (CI: −1.4; −0.1) and −1.06 (CI: −1.8; −0.3) and gross motor; mean z-score difference: −0.87 (CI: −1.7; −0.1) and −1.22 (CI: −2.4; −0.02) categories.

Conclusions:

The children with CHD achieved lower scores in the Bayley Scales cognition category and the Ages and Stages Questionnaire communication and gross motor categories possibly indicative of early neurodevelopmental deficiencies. We recommend early screening and monitoring for neurodevelopmental delays in children with CHD in order to improve further neurodevelopment and educational achievements.

Type
Original Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

CHDs are the most common major birth defects worldwide, affecting 6 to 8 children per 1000 live births with 3 per 1000 requiring surgical or catheter-based intervention early in life.Reference Hoffman and Kaplan1,Reference Dolk, Loane and Garne2 Earlier diagnostics, improved treatment, and perioperative care have resulted in higher survival ratesReference Gilboa, Salemi, Nembhard, Fixler and Correa3Reference Oster, Lee, Honein, Riehle-Colarusso, Shin and Correa5 with more adults than children living with CHD today.Reference Bhatt, Foster and Kuehl6,Reference Dearani, Connolly, Martinez, Fontanet and Webb7 The focus on clinical outcome has therefore shifted from early mortality to long-term morbidity. In recent years, studies have shown that children born with CHD have increased risk of neurodevelopmental deficiencies (such as deficits in language development, social skills, executive functioning, and motor skills)Reference Cassidy, White, DeMaso, Newburger and Bellinger8Reference Wernovsky14 compared to the background population, and that these neurodevelopmental deficiencies persist in adolescence and adulthood with an increase in psychiatric diagnoses, lower educational achievements, and reduced work participation.Reference Udholm, Nyboe, Dantoft, Jørgensen, Rask and Hjortdal15Reference Nyboe, Fonager, Larsen, Andreasen, Lundbye-Christensen and Hjortdal17 It is estimated that 33–43% of children born with a major CHD will suffer from impaired neurocognitive development,Reference Bellinger, Wypij and Rivkin9,Reference Khalil, Suff, Thilaganathan, Hurrell, Cooper and Carvalho18 thus making neurodevelopmental deficiencies the most common long-term morbidity in these patients.Reference Gaynor, Stopp and Wypij19 While the association between CHD and educational achievement in Danish adolescents has been studied by Olsen et al, 2011Reference Olsen, Hjortdal, Mortensen, Christensen, Sørensen and Pedersen16, a systematic early neurocognitive blinded follow-up study in Danish children with and without isolated CHD has, to our knowledge, yet to be performed. Early screenings and monitoring for neurodevelopmental deficiencies in this patient group will help facilitate proper and early intervention and support for both child and family and hereby give the child the best possible chances for optimal neurodevelopment.Reference Asschenfeldt, Evald and Heiberg20,Reference Peyvandi, Chau and Guo21

According to the American Heart AssociationReference Marino, Lipkin and Newburger22 and recently the Cardiac Neurodevelopmental Outcome Collaborative,Reference Ware, Butcher and Latal23 early detection of neurodevelopmental deficiencies is of utter importance to the child’s further development and educational achievements. To our knowledge, a neurocognitive screening programme for this patient group is yet to be established in Denmark.

The aim of this cohort study was to investigate the early neurocognitive development in 15 Danish children born with isolated CHD compared with 27 Danish contemporary and age-equivalent children without CHD at 18 and 36 months using the Bayley Scales of Infant and Toddler Development (3rd edition)Reference Bayley24 according to age and the Ages and Stages Questionnaire (3rd edition)Reference Squires25 according to age and 6 months above age. The latter was used in order to discover if above-age challenges would be more sensitive to differences between the groups.Reference Plomgaard, Hansen and Greisen26

Materials and methods

Study design and recruitment

This study is an ongoing prospective cohort study including fetal and neonatal MRIReference Lauridsen, Uldbjerg and Henriksen27,Reference Skotting, Eskildsen and Ovesen28 as well as neurodevelopmental follow-up. The study is taking place at Aarhus University Hospital, Denmark. We here present the neurodevelopmental follow-up using the Bayley Scales of Infant and Toddler Development (3rd edition) and the Ages and Stages Questionnaire (3rd edition) on the same cohort of children with and without CHD.

Initial cohort

Recruitment took place before birth. Women expecting fetuses with and without isolated heart defects were recruited at Aarhus University Hospital between October 2014 and June 2016. The women expecting children with CHD were approached by the obstetric physician at the time of prenatal diagnosis. The women expecting fetuses without heart defects were approached randomly at the first or second routine, free of charge, prenatal ultrasound scan offered all pregnant women in Denmark at approximately gestational age week 12 and 20. The initial cohort consisted of 16 singleton fetuses with isolated CHDs believed to cause disturbances in the flow of oxygenated blood to the fetal brain and 40 singleton fetuses without CHDs. Exclusion criteria in both groups were multiple gestation, chromosomal, genetic, or multiple abnormalities, language other than Danish, social matters, claustrophobia, and birth prior to intrauterine MRI. The women underwent fetal MRI twice during pregnancy.Reference Lauridsen, Uldbjerg and Henriksen27

Study size and final cohort

After birth, both parents were asked to give written informed consent to continue participation and include their newborn in the present postnatal follow-up study. One child with CHD died before follow-up (see Fig 1) and 13 of the 40 children without CHD declined to participate. Thus, loss to follow-up was 6% among those with CHD and 33% among those without. For the demographic data see Table 1, for CHD types and age of surgery see Table 2.

Figure 1. Flowchart illustrating the recruitment of fetuses with heart defects. n indicates the number of children.

Table 1. Maternal and newborn characteristics in 15 pregnancies with isolated fetal heart defects and 27 pregnancies without fetal heart defects

Maternal and newborn characteristics in 15 children with heart defects and 27 children without heart defects, Aarhus Denmark 2014–2016. Data are presented as median (interquartile range) or n (%) or mean (SD). n indicates number. Despite extensive search, we did not have information on educational attainment from all participants

Table 2. CHD and surgery characteristics in 15 children with CHD

CHD and surgery characteristics in 15 children with heart defects, Aarhus Denmark 2014–2016. Data are presented as n (%) or median (interquartile range). n = number; TGA = transposition of the great arteries; VSD = ventricular septal defect

Twelve of the 15 children with CHD underwent prenatal genetic testing; karyotype (n = 2) and array-based comparative genomic hybridization (n = 11 – including one, who had already had a karyotype and one including a single-nucleotide polymorphism analyses). Only one minor abnormality of no clinical significance was detected. The remaining three children with CHD and the 27 children without CHD did not undergo genetic evaluation; however, none of them showed any clinical signs of genetic, chromosomal, or syndromic disorders.

One mother expecting a child without CHD was treated for pregnancy hypertension.

Quantitative variables and the tests

After birth, information on birth weight, birth length, head circumference, placenta weight, and gestational age were collected (see Table 1).

The follow-up presented in the present study includes the Bayley Scales of Infant and Toddler Development 3rd edition assessments (designed to asses developmental functioning of children aged 1 to 42 months through structured play)Reference Bayley24 at 18 and 36 months of age. The children were tested in the three domains: cognitive, language, and motor. As far as it was possible, the therapists were blinded to whether the child had CHD or not. The administration of the tests followed manual guidelines with optimal test conditions in place. At 18 and 36 months, the parents also completed the Ages and Stages Questionnaire 3rd edition.Reference Squires25

The Ages and Stages Questionnaire is a self-administered (parents) 30-item screening questionnaire related to child development from 1 month to 5 years of age. The items cover five domains of development: communication, gross and fine motor skills, problem-solving, and personal-social issues.Reference Squires25

When Ages and Stages Questionnaire is used as a screening tool, children who perform better-than-average will score near maximum. This results in an underestimation of the mean. To get a normal distribution of the scores, the children were therefore given questionnaires meant for a 6-month-older child.Reference Plomgaard, Hansen and Greisen26

Reference values of both the Ages and Stages Questionnaire and the Bayley Scales of Infant and Toddler Development assessment are based on the performance of American children.Reference Bayley24,Reference Squires25 In the Bayley Scales 3rd edition, 9.8% of the normative sample were clinical cases.Reference Bayley24 Results were included if the child participated in at least one of the planned examinations.

Statistics

From each of the three domains in the Bayley Scales of Infant and Toddler Development test, a composite raw score was achieved, and this raw score was converted to a scale score according to normative data disclosed in the Bayley Scales manual.Reference Bayley24 The mean scale score is 100, and one standard deviation corresponds to 15 scale points.Reference Bayley24 For statistical analysis purposes, Van Chau and colleagues (2013)Reference Chau, Synnes, Grunau, Poskitt, Brant and Miller29 suggested a novel classification of the scale score into four scale score categories given previous findings that the Bayley-III seems to overestimate neurodevelopmentReference Acton, Biggs and Creighton30: normal (>100), low normal (85–100), mild impairment (70–84), and significant impairment (<70).

From each of the five domains in the Ages and Stages Questionnaire, a score was achieved and the corresponding z-scores were calculated according to normative data disclosed in the manual.Reference Squires25

We used Student’s t-test and z-test to calculate the mean difference between the results of the Bayley Scales assessments and the Ages and Stages Questionnaire presented with 95% confidence intervals (CIs).

Ethics

The study was approved by the Danish Data Protection Agency (chart: 1–16–02–86–14) and by the National Committee on Health Research, Denmark (chart: 1–10–72–61–14). The protocol of the project conforms to the ethical standards of the Helsinki Declaration revised in 2008.

Results

The final cohort consisted of 42 children, 15 with isolated CHD and 27 without. Table 1 shows maternal and newborn characteristics and Table 2 shows CHD and surgery details.

At the mean age of 18 months and 8 days (standard deviation: 21 days) and at the mean age of 36 months and 28 days (standard deviation: 46 days), respectively, a physiotherapist and an occupational therapist performed the Bayley Scales of Infant and Toddler Development (3rd edition) assessments at Aarhus University Hospital. The neurodevelopmental test results are presented in Tables 3 and 4.

Table 3. The Bayley Scales of Infant and Toddler Development and the Ages and Stages Questionnaire test results at, respectively, 18 months and 36 months in 15 children with isolated CHD and 27 without CHD

Data are presented as mean (SD). Measures were compared by Student’s t-test and z-test. CI indicates 95% confidence interval; Bayley-III, the Bayley Scales of Infant and Toddler Development-Third Edition; ASQ-3, the Ages and Stages Questionnaires Third Edition; n = the number of children in each group; N = the number of measurements in each group.

* Statistical significance at p < 0.05

Table 4. The Bayley Scales of Infant and Toddler Development composite scale scores descriptive classification relative risk at 18 and 36 months in 15 children with CHD

Data are presented as relative risk (CI). Bayley-III indicates the Bayley Scales of Infant and Toddler Development-Third Edition; CI = confidence interval.

* Statistical significance at p < 0.05

In the Bayley Scales of Infant and Toddler Development assessments at 18 and 36 months, we were not able to detect performance difference between the children with and without CHD when comparing mean scale scores in the different categories.

Table 4 shows the relative risk (CI) of scoring normal (>100), low normal (85–100), mild impairment (70–84), or significant impairment (<70).Reference Chau, Synnes, Grunau, Poskitt, Brant and Miller29 Additionally, we calculated the risk of scoring below normal (≤100) compared to normal. Children with CHD had, compared with the children without CHD, an increased risk of scoring below normal in the Bayley Scales cognition category at 18 and 36 months; relative risk 1.7 (95% CI: 1.0–2.8) and 3.1 (CI: 1.2–7.5), respectively. See Fig 2 for a histogram of the distribution of the children.

Figure 2. The Bayley Scales of Infant and Toddler Development scale scores descriptive classifications at 18 and 36 months in 15 children with CHD and 27 without CHD. Bayley-III indicates the Bayley Scales of Infant and Toddler Development-Third Edition.

In both the Bayley Scales assessments, the children with CHD were on average a little older than the children without CHD: +9 days at the 18-month and +25 days at the 36-month assessment.

At 18 and 36 months, the parents completed each time two sets of the Ages and Stages Questionnaire (3rd edition). The Ages and Stages Questionnaire according to age (see Supplementary Table S1) showed that the children with CHD achieved lower communication scores at 36 months of age. When challenged with the milestones of a 6-month-older child, these performance differences persisted as those with CHD achieved lower scores than the children without CHD in the communication and gross motor categories at both follow-ups; communication mean z-score difference −0.72 (CI: −1.4; −0.1) and −1.06 (CI: −1.8; −0.3) and gross motor; mean z-score difference: −0.87 (CI: −1.7; −0.1) and −1.22 (CI: −2.4; −0.02), respectively (see Table 3 for details).

Discussion

Key results

The children with major isolated CHD had an up to three times higher risk of scoring below normal in the Bayley Scales of Infant and Toddler Development (3rd edition) cognition category.

Additionally, children with CHD achieved lower scores than their age-equivalent peers in the Ages and Stages Questionnaire (3rd edition) communication and gross motor categories, and this performance difference persisted over time.

Interpretation

Our findings indicates that children with CHD have cognitive challenges. In addition, the parents find that the children with CHD are challenged in the communication and gross motor categories compared to their age-equivalent peers. And the neurodevelopmental challenges in children with CHD persist over time. We may only see the tip of the iceberg in our cohort. The significance of the neurodevelopmental deficiencies may increase when the children are growing and experience increasing demands of skills and capabilities. Their skills might be sufficient at 36 months, but these children are at risk of lacking behind when starting school and the complexity of the educational curriculum increases.Reference Olsen, Hjortdal, Mortensen, Christensen, Sørensen and Pedersen16,Reference Asschenfeldt, Evald and Heiberg20,Reference Majnemer, Limperopoulos, Shevell, Rosenblatt, Rohlicek and Tchervenkov31,Reference Bellinger, Wypij and duPlessis32 Brosig et al, 2018Reference Brosig, Bear and Allen33 found that many of their patients who scored in the average range at 2 years of age showed deficits at 4 years of age.

In the present study, we demonstrate that motor and communication deviations are detectable using the Ages and Stages Questionnaire already in early childhood in line with previous research,Reference Gaynor, Stopp and Wypij19,Reference Latal34Reference Brandlistuen, Stene-Larsen, Holmstrom, Landolt, Eskedal and Vollrath37 and that the children with CHD have a higher risk of scoring below normal in the Bayley Scales cognition category at 18 and 36 months.

The Ages and Stages Questionnaire (3rd edition) has been tested in different high-risk patient groupsReference Skellern, Rogers and O’Callaghan38Reference Lindsay, Healy, Colditz and Lingwood40 and has been validated in different countries, languages, and settings.Reference Richter and Janson41Reference Elbers, Macnab, McLeod and Gagnon43 In the CHD patient group, Noeder et al, 2017Reference Noeder, Logan and Struemph44 found the Ages and Stages Questionnaire to be a valid screening tool, especially in the gross motor category where they found excellent sensitivity.

We found that only the Ages and Stages Questionnaire could detect performance differences between the two groups when comparing mean scale scores in the different categories. For some of the children with isolated CHD, where the parent’s response to the Ages and Stages Questionnaire indicated potential neurodevelopmental delay, we found no definite signs of delay in the Bayley Scales assessments. However, these children may still represent a group at-risk for future neurodevelopmental deficiencies,Reference Schonhaut, Armijo, Schonstedt, Alvarez and Cordero45 and this is supported by the fact that the children with CHD had an up to three times increased risk of scoring below normal in the Bayley Scales 3rd edition cognition category. Borderline intellectual functioning has been connected to limitations in social and behavioral capacities in childhood.Reference Blasi, Pirastru and Cabinio46,Reference Baglio, Blasi and Intra47

It is possible that we, with a larger study cohort, would have been able to detect more differences between the children with and without CHD.

The Bayley Scales of Infant and Toddler Development is by many considered the gold standard of infant developmental assessment and is among the most frequently used standardised instruments for assessing early neurodevelopment in preschool children. However, the Bayley Scales of Infant and Toddler Development 3rd editionReference Bayley24 were published in 2006, and several studies have later argued that the 3rd edition underestimates delays by overestimating the children’s developmentReference Chau, Synnes, Grunau, Poskitt, Brant and Miller29,Reference Acton, Biggs and Creighton30,Reference Long, Galea, Eldridge and Harris48Reference Johnson, Moore and Marlow53 and when using the Bayley Scales to describe neurodevelopment in early preschool years, caution is warranted.Reference Ware, Butcher and Latal23 This and our use of an Ages and Stages Questionnaire designed for a 6-month-older child might offer an explanation to why we observe more children at risk using Ages and Stages Questionnaire than with the Bayley Scales of Infant and Toddler Development 3rd edition. It is likely that an overestimation of the children’s abilities will affect the poorest performers the most, thus making the children with neurodevelopmental challenges appear to perform better than they actually do.Reference Goldstone, Baiocchi and Wypij50 We have tried to accommodate this overestimation by using the categories suggested by Van Chau and colleagues.Reference Chau, Synnes, Grunau, Poskitt, Brant and Miller29

Limitations

An important limitation is the small group sizes and the heterogenicity of the CHDs included in the study and hence a big difference in the complexity of the surgeries the children with CHD have undergone. The fact that the children without CHD are more than a month older than those with CHD at the time of the late Ages and Stages Questionnaire assessment is also a limitation that probably leads to an overestimation of the difference between the groups.

Strengths

A major strength in our study is that we within the same time period have included and examined age-equivalent peers without CHD. Because of our use of a reference group, confounding variables known to affect neurocognitive development such as, for example, birth weight, gestation age, and maternal education can be minimised. The children with CHD and the reference group are very similar in regard to maternal characteristics and hence socio-economic status. Another big strength worth mentioning is the exclusion of children with both syndromic CHD and genetic abnormalities, since many genetic syndromes are connected with impaired neurocognitive development, and the inclusion of these children may therefore distort the results. We have included children with transposition of the great arteries, but also children with coarctation/hypoplastic arch not so often included in follow-up studies,Reference Cassidy, White, DeMaso, Newburger and Bellinger8Reference Calderon, Angeard, Pinabiaux, Bonnet and Jambaque11,Reference Peyvandi, Chau and Guo21,Reference Hiraiwa, Ibuki and Tanaka54 and we still find differences between the children with and without CHD indicative of neurodevelopmental deficiencies. This indicates that probably all children with CHD would benefit from systematic follow-up in order to initiate relevant support to the families. The occupational and physiotherapist were blinded as far as possible to whether or not the child had a CHD while assessing the children, and this also strengthen the results of this study. Furthermore, the children in this study have undergone a comprehensive multidimensional neurodevelopmental assessment comprising of both parental reports, direct child testing, and clinical observations as recommended by the Cardiac Neurodevelopmental Outcome Collaborative.Reference Ware, Butcher and Latal23

Generalisability

Both the guidelines from the American Heart AssociationReference Marino, Lipkin and Newburger22 and from the Cardiac Neurodevelopmental Outcome CollaborativeReference Ware, Butcher and Latal23 state the importance of screening and continuously monitoring all children born with CHD for neurodevelopmental impairment. Not just children born with major CHD, but the entire cohort of children and adolescents with CHD. In Denmark, such screening has yet to be established. Based on the results in this present study and in previous studies, we strongly recommend that an extensive screening and monitoring programme is to be established in Denmark, to give these children and families the support they need in order for the children to reach their full potential.

Supplementary material

To view supplementary material for this article, please visit https://doi.org/10.1017/S1047951121002195

Acknowledgements

The authors thank the children and families who participated in this study. We would also like to thank Niels Uldbjerg, MD, DMSc1, Olav Bjørn Pedersen, MD2, PhD, and Camilla Linddahl, MD1, for the help with recruitment. 1Department of Gynecology and Obstetrics, Aarhus University Hospital, Aarhus, Denmark, and 2Department of Gynecology and Obstetrics, Copenhagen University Hospital, Denmark.

Financial support

This study received financial support from the Danish Children’s Heart Foundation (Børnehjertefonden) (M.H.L., grant number 100,000 DKK) and Frimodt Heineke Fonden (M.H.L., grant number 50,000 DKK).

Conflicts of interest

None.

Ethical standards

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national guidelines on human experimentation (the National Committee on Health Research, Denmark and the Danish Data Protection Agency), and with the Helsinki Declaration of 1975, as revised in 2008, and have been approved by the institutional committees (the National Committee on Health Research, Denmark).

References

Hoffman, JI, Kaplan, S. The incidence of congenital heart disease. J Am Coll Cardiol. 2002; 39: 18901900. doi: 10.1016/s0735-1097(02)01886-7.CrossRefGoogle ScholarPubMed
Dolk, H, Loane, M, Garne, E. Congenital heart defects in Europe: prevalence and perinatal mortality, 2000 to 2005. Circulation. 2011; 123: 841849. doi: 10.1161/circulationaha.110.958405.CrossRefGoogle ScholarPubMed
Gilboa, SM, Salemi, JL, Nembhard, WN, Fixler, DE, Correa, A. Mortality resulting from congenital heart disease among children and adults in the United States, 1999 to 2006. Circulation. 2010; 122: 22542263. doi: 10.1161/circulationaha.110.947002.CrossRefGoogle ScholarPubMed
Boneva, RS, Botto, LD, Moore, CA, Yang, Q, Correa, A, Erickson, JD. Mortality associated with congenital heart defects in the United States: trends and racial disparities, 1979–1997. Circulation. 2001; 103: 23762381. doi: 10.1161/01.cir.103.19.2376.CrossRefGoogle ScholarPubMed
Oster, ME, Lee, KA, Honein, MA, Riehle-Colarusso, T, Shin, M, Correa, A. Temporal trends in survival among infants with critical congenital heart defects. Pediatrics. 2013; 131: e15021508. doi: 10.1542/peds.2012-3435.CrossRefGoogle ScholarPubMed
Bhatt, AB, Foster, E, Kuehl, K, et al. Congenital heart disease in the older adult: a scientific statement from the American Heart Association. Circulation. 2015; 131: 18841931, doi: 10.1161/cir.0000000000000204.CrossRefGoogle ScholarPubMed
Dearani, JA, Connolly, HM, Martinez, R, Fontanet, H, Webb, GD. Caring for adults with congenital cardiac disease: successes and challenges for 2007 and beyond. Cardiol Young. 2007; 17 (Suppl 2): 8796. doi: 10.1017/s1047951107001199.CrossRefGoogle ScholarPubMed
Cassidy, AR, White, MT, DeMaso, DR, Newburger, JW, Bellinger, DC. Executive function in children and adolescents with critical cyanotic congenital heart disease. J Int Neuropsychol Soc. 2015; 21: 3449. doi: 10.1017/s1355617714001027.CrossRefGoogle ScholarPubMed
Bellinger, DC, Wypij, D, Rivkin, MJ, et al. Adolescents with d-transposition of the great arteries corrected with the arterial switch procedure: neuropsychological assessment and structural brain imaging. Circulation. 2011; 124: 13611369. doi: 10.1161/circulationaha.111.026963.CrossRefGoogle ScholarPubMed
Oberhuber, RD, Huemer, S, Mair, R, Sames-Dolzer, E, Kreuzer, M, Tulzer, G. Cognitive development of school-age hypoplastic left heart syndrome survivors: a single center study. Pediatr Cardiol. 2017; 38: 10891096. doi: 10.1007/s00246-017-1623-8.CrossRefGoogle ScholarPubMed
Calderon, J, Angeard, N, Pinabiaux, C, Bonnet, D, Jambaque, I. Facial expression recognition and emotion understanding in children after neonatal open-heart surgery for transposition of the great arteries. Dev Med Child Neurol. 2014; 56: 564571. doi: 10.1111/dmcn.12381.CrossRefGoogle ScholarPubMed
Ricci, MF, Andersen, JC, Joffe, AR, et al. Chronic neuromotor disability after complex cardiac surgery in early life. Pediatrics. 2015; 136: e922e933. doi: 10.1542/peds.2015-1879.CrossRefGoogle ScholarPubMed
Gerstle, M, Beebe, DW, Drotar, D, Cassedy, A, Marino, BS. Executive functioning and school performance among pediatric survivors of complex congenital heart disease. J Pediatr. 2016; 173: 154159. doi: 10.1016/j.jpeds.2016.01.028.CrossRefGoogle ScholarPubMed
Wernovsky, G. Current insights regarding neurological and developmental abnormalities in children and young adults with complex congenital cardiac disease. Cardiol Young. 2006; 16 (Suppl 1): 92104. doi: 10.1017/s1047951105002398.CrossRefGoogle Scholar
Udholm, S, Nyboe, C, Dantoft, TM, Jørgensen, T, Rask, CU, Hjortdal, VE. Small atrial septal defects are associated with psychiatric diagnoses, emotional distress, and lower educational levels. Congenital Heart Dis 2019; 14: 803810. doi: 10.1111/chd.12808.CrossRefGoogle ScholarPubMed
Olsen, M, Hjortdal, VE, Mortensen, LH, Christensen, TD, Sørensen, HT, Pedersen, L. Educational achievement among long-term survivors of congenital heart defects: a Danish population-based follow-up study. Cardiol Young. 2011; 21: 197203. doi: 10.1017/s1047951110001769.CrossRefGoogle ScholarPubMed
Nyboe, C, Fonager, K, Larsen, ML, Andreasen, JJ, Lundbye-Christensen, S, Hjortdal, V. Effect of atrial septal defect in adults on work participation (from a nation wide register-based follow-up study regarding work participation and use of permanent social security benefits). Am J Cardiol. 2019; 124: 17751779. doi: 10.1016/j.amjcard.2019.08.041.CrossRefGoogle Scholar
Khalil, A, Suff, N, Thilaganathan, B, Hurrell, A, Cooper, D, Carvalho, JS. Brain abnormalities and neurodevelopmental delay in congenital heart disease: systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2014; 43: 1424. doi: 10.1002/uog.12526.CrossRefGoogle ScholarPubMed
Gaynor, JW, Stopp, C, Wypij, D, et al. Neurodevelopmental outcomes after cardiac surgery in infancy. Pediatrics. 2015; 135: 816825. doi: 10.1542/peds.2014-3825.CrossRefGoogle ScholarPubMed
Asschenfeldt, B, Evald, L, Heiberg, J, et al. Neuropsychological status and structural brain imaging in adults with simple congenital heart defects closed in childhood. J Am Heart Assoc. 2020. doi: 10.1161/jaha.120.015843.CrossRefGoogle ScholarPubMed
Peyvandi, S, Chau, V, Guo, T, et al. Neonatal brain injury and timing of neurodevelopmental assessment in patients with congenital heart disease. J Am Coll Cardiol. 2018; 71: 19861996. doi: 10.1016/j.jacc.2018.02.068.CrossRefGoogle ScholarPubMed
Marino, BS, Lipkin, PH, Newburger, JW, et al. Neurodevelopmental outcomes in children with congenital heart disease: evaluation and management: a scientific statement from the American Heart Association. Circulation. 2012; 126: 11431172. doi: 10.1161/CIR.0b013e318265ee8a.CrossRefGoogle ScholarPubMed
Ware, J, Butcher, JL, Latal, B, et al. Neurodevelopmental evaluation strategies for children with congenital heart disease aged birth through 5 years: recommendations from the cardiac neurodevelopmental outcome collaborative. Cardiol Young. 2020; 30: 16091622. doi: 10.1017/S1047951120003534.CrossRefGoogle ScholarPubMed
Bayley, N. Bayley Scales of Infant and Toddler Development Third Edition Administration Manual. NCS Pearson, Inc., San Antonio, TX, 2006.Google Scholar
Squires, J. Ages and Stages Questionnaires Third Edition User’s Guide. Paul H. Brookes Publishing Co., Inc., Baltimore, MD, 2009.CrossRefGoogle Scholar
Plomgaard, AM, Hansen, BM, Greisen, G. Measuring developmental deficit in children born at gestational age less than 26 weeks using a parent-completed developmental questionnaire. Acta Paediatr 2006; 95: 14881494. doi: 10.1080/08035250600684438.CrossRefGoogle ScholarPubMed
Lauridsen, MH, Uldbjerg, N, Henriksen, TB, et al. Cerebral oxygenation measurements by magnetic resonance imaging in fetuses with and without heart defects. Circ Cardiovasc Imaging 2017; 10: e006459. doi: 10.1161/circimaging.117.006459.CrossRefGoogle ScholarPubMed
Skotting, MB, Eskildsen, SF, Ovesen, AS, et al. Infants with congenital heart defects have reduced brain volumes. Sci Rep. 2021; 11: 4191. doi: 10.1038/s41598-021-83690-3.CrossRefGoogle ScholarPubMed
Chau, V, Synnes, A, Grunau, RE, Poskitt, KJ, Brant, R, Miller, SP. Abnormal brain maturation in preterm neonates associated with adverse developmental outcomes. Neurology. 2013; 81: 20822089. doi: 10.1212/01.wnl.0000437298.43688.b9.CrossRefGoogle ScholarPubMed
Acton, BV, Biggs, WSG, Creighton, DE, et al. Overestimating neurodevelopment using the Bayley-III after early complex cardiac surgery. Pediatrics. 2011; 128, e794e800. doi: 10.1542/peds.2011-0331.CrossRefGoogle Scholar
Majnemer, A, Limperopoulos, C, Shevell, M, Rosenblatt, B, Rohlicek, C, Tchervenkov, C. Long-term neuromotor outcome at school entry of infants with congenital heart defects requiring open-heart surgery. J Pediatr. 2006; 148: 7277. doi: 10.1016/j.jpeds.2005.08.036.CrossRefGoogle ScholarPubMed
Bellinger, DC, Wypij, D, duPlessis, AJ, et al. Neurodevelopmental status at eight years in children with dextro-transposition of the great arteries: the Boston Circulatory Arrest Trial. J Thorac Cardiovasc Surg. 2003; 126: 13851396. doi: 10.1016/s0022-5223(03)00711-6.CrossRefGoogle ScholarPubMed
Brosig, CL, Bear, L, Allen, S, et al. Neurodevelopmental outcomes at 2 and 4 years in children with congenital heart disease. Congenital Heart Dis. 2018; 13: 700705. doi: 10.1111/chd.12632.CrossRefGoogle ScholarPubMed
Latal, B. Neurodevelopmental outcomes of the child with congenital heart disease. Clin Perinatol. 2016; 43: 173185. doi: 10.1016/j.clp.2015.11.012.CrossRefGoogle ScholarPubMed
Laraja, K, Sadhwani, A, Tworetzky, W, et al. Neurodevelopmental outcome in children after fetal cardiac intervention for aortic stenosis with evolving hypoplastic left heart syndrome. J Pediatr. 2017; 184: 130136.e134. doi: 10.1016/j.jpeds.2017.01.034.CrossRefGoogle ScholarPubMed
Campbell, MJ, Ziviani, JM, Stocker, CF, Khan, A, Sakzewski, L. Neuromotor performance in infants before and after early open-heart surgery and risk factors for delayed development at 6 months of age. Cardiol Young. 2019; 29: 100109. doi: 10.1017/s1047951118001622.CrossRefGoogle ScholarPubMed
Brandlistuen, RE, Stene-Larsen, K, Holmstrom, H, Landolt, MA, Eskedal, LT, Vollrath, ME. Motor and social development in 6-month-old children with congenital heart defects. J Pediatr. 2010; 156: 265269.e261. doi: 10.1016/j.jpeds.2009.08.035.CrossRefGoogle ScholarPubMed
Skellern, CY, Rogers, Y, O’Callaghan, MJ. A parent-completed developmental questionnaire: follow up of ex-premature infants. J Paediatr Child Health. 2001; 37: 125129. doi: 10.1046/j.1440-1754.2001.00604.x.CrossRefGoogle ScholarPubMed
Klamer, A, Lando, A, Pinborg, A, Greisen, G. Ages and stages questionnaire used to measure cognitive deficit in children born extremely preterm. Acta Paediatr. 2005; 94: 13271329. doi: 10.1111/j.1651-2227.2005.tb02095.x.CrossRefGoogle ScholarPubMed
Lindsay, NM, Healy, GN, Colditz, PB, Lingwood, BE. Use of the ages and stages questionnaire to predict outcome after hypoxic-ischaemic encephalopathy in the neonate. J Paediatr Child Health. 2008; 44: 590595. doi: 10.1111/j.1440-1754.2008.01388.x.CrossRefGoogle ScholarPubMed
Richter, J, Janson, H. A validation study of the Norwegian version of the ages and stages questionnaires. Acta Paediatr. 2007; 96: 748752. doi: 10.1111/j.1651-2227.2007.00246.x.CrossRefGoogle ScholarPubMed
Juneja, M, Mohanty, M, Jain, R, Ramji, S. Ages and stages questionnaire as a screening tool for developmental delay in Indian children. Indian Pediatr. 2012; 49: 457461. doi: 10.1007/s13312-012-0074-9.CrossRefGoogle ScholarPubMed
Elbers, J, Macnab, A, McLeod, E, Gagnon, F. The ages and stages questionnaires: feasibility of use as a screening tool for children in Canada. Can J Rural Med. 2008; 13: 914.Google ScholarPubMed
Noeder, MM, Logan, BA, Struemph, KL, et al. Developmental screening in children with CHD: ages and stages questionnaires. Cardiol Young. 2017; 27: 14471454. doi: 10.1017/s1047951117000415.CrossRefGoogle ScholarPubMed
Schonhaut, L, Armijo, I, Schonstedt, M, Alvarez, J, Cordero, M. Validity of the ages and stages questionnaires in term and preterm infants. Pediatrics. 2013; 131: e14681474. doi: 10.1542/peds.2012-3313.CrossRefGoogle ScholarPubMed
Blasi, V, Pirastru, A, Cabinio, M, et al. Early life adversities and borderline intellectual functioning negatively impact limbic system connectivity in childhood: a connectomics-based study. Front Psychiatry. 2020; 11: 497116. doi: 10.3389/fpsyt.2020.497116.CrossRefGoogle ScholarPubMed
Baglio, G, Blasi, V, Intra, FS, et al. Social competence in children with borderline intellectual functioning: delayed development of theory of mind across all complexity levels. Front Psychol. 2016; 7: 1604. doi: 10.3389/fpsyg.2016.01604.CrossRefGoogle ScholarPubMed
Long, SH, Galea, M, Eldridge, BJ, Harris, SR. Performance of 2-year-old children after early surgery for congenital heart disease on the Bayley Scales of Infant and Toddler development, third edition. Early Hum Dev. 2012; 88: 603607. doi: 10.1016/j.earlhumdev.2012.01.007.CrossRefGoogle ScholarPubMed
Anderson, PJ, De Luca, CR, Hutchinson, E, Roberts, G, Doyle, LW. Underestimation of developmental delay by the new Bayley-III Scale. Arch Pediatr Adolesc Med. 2010; 164: 352356. doi: 10.1001/archpediatrics.2010.20.CrossRefGoogle ScholarPubMed
Goldstone, AB, Baiocchi, M, Wypij, D, et al. The Bayley-III scale may underestimate neurodevelopmental disability after cardiac surgery in infants. Eur J Cardiothorac Surg. 2020; 57: 6371. doi: 10.1093/ejcts/ezz123.CrossRefGoogle ScholarPubMed
Jary, S, Whitelaw, A, Walloe, L, Thoresen, M. Comparison of Bayley-2 and Bayley-3 scores at 18 months in term infants following neonatal encephalopathy and therapeutic hypothermia. Dev Med Child Neurol. 2013; 55: 10531059. doi: 10.1111/dmcn.12208.CrossRefGoogle ScholarPubMed
Lowe, JR, Erickson, SJ, Schrader, R, Duncan, AF. Comparison of the Bayley II mental developmental index and the Bayley III cognitive scale: are we measuring the same thing? Acta Paediatr. 2012; 101: e55e58. doi: 10.1111/j.1651-2227.2011.02517.x.CrossRefGoogle ScholarPubMed
Johnson, S, Moore, T, Marlow, N. Using the Bayley-III to assess neurodevelopmental delay: which cut-off should be used? Pediatr Res. 2014; 75: 670674. doi: 10.1038/pr.2014.10.CrossRefGoogle ScholarPubMed
Hiraiwa, A, Ibuki, K, Tanaka, T, et al. Toddler neurodevelopmental outcomes are associated with school-age IQ in children with single ventricle physiology. Semin Thorac Cardiovasc Surg. 2019. doi: 10.1053/j.semtcvs.2019.10.017.Google ScholarPubMed
Figure 0

Figure 1. Flowchart illustrating the recruitment of fetuses with heart defects. n indicates the number of children.

Figure 1

Table 1. Maternal and newborn characteristics in 15 pregnancies with isolated fetal heart defects and 27 pregnancies without fetal heart defects

Figure 2

Table 2. CHD and surgery characteristics in 15 children with CHD

Figure 3

Table 3. The Bayley Scales of Infant and Toddler Development and the Ages and Stages Questionnaire test results at, respectively, 18 months and 36 months in 15 children with isolated CHD and 27 without CHD

Figure 4

Table 4. The Bayley Scales of Infant and Toddler Development composite scale scores descriptive classification relative risk at 18 and 36 months in 15 children with CHD

Figure 5

Figure 2. The Bayley Scales of Infant and Toddler Development scale scores descriptive classifications at 18 and 36 months in 15 children with CHD and 27 without CHD. Bayley-III indicates the Bayley Scales of Infant and Toddler Development-Third Edition.

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