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Cited by 59Congenital Heart Disease StudiesNeonatal and fetal brain pathologyFetal and Pediatric Neurological Disorders

Neuroimaging, cardiovascular physiology, and functional outcomes in infants with congenital heart disease

Open access
Claessens, Nathalie H P, Kelly, Christopher J, Counsell, Serena J, Benders, Manon J N L·2017·Developmental Medicine & Child Neurology
DOI 10.1111/dmcn.13461
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Abstract

This review integrates data on brain dysmaturation and acquired brain injury using fetal and neonatal magnetic resonance imaging (MRI), including the contribution of cardiovascular physiology to differences in brain development, and the relationship between brain abnormalities and subsequent neurological impairments in infants with congenital heart disease (CHD). The antenatal and neonatal period are critical for optimal brain development; the developing brain is particularly vulnerable to haemodynamic disturbances during this time. Altered cerebral perfusion and decreased cerebral oxygen delivery in the antenatal period can affect functional and structural brain development, while postnatal haemodynamic fluctuations may cause additional injury. In critical CHD, brain dysmaturation and acquired brain injury result from a combination of underlying cardiovascular pathology and surgery performed in the neonatal period. MRI findings in infants with CHD can be used to evaluate potential clinical risk factors for brain abnormalities, and aid prediction of functional outcomes at an early stage. In addition, information on timing of brain dysmaturation and acquired brain injury in CHD has the potential to be used when developing strategies to optimize neurodevelopment.

AI snapshot

Written from the paper’s full text.

TL;DR

This review synthesizes fetal and neonatal MRI evidence showing that infants with critical congenital heart disease have brain dysmaturation and acquired brain injury linked to altered cardiovascular physiology and cerebral oxygen delivery. It argues these early brain abnormalities likely contribute to later motor, cognitive, and behavioral deficits, but long-term outcome data remain limited.

Key findings

  • In late gestation, fetuses with left or right outflow tract obstruction (n=30) had a 10% reduction in cerebral blood oxygen saturation versus healthy fetuses, corresponding to a 15% reduction in cerebral oxygen delivery and a 32% reduction in cerebral oxygen consumption.
  • Before neonatal surgery, cerebral blood flow was comparable among neonates with SVP, TGA, and coarctation (n=32) and healthy controls (n=31), but oxygen delivery was reduced in SVP and TGA; arterial oxygen saturation was 98% in controls, 98% in coarctation, 84% in SVP, and 86% in TGA.
  • Fetal and neonatal MRI studies consistently show reduced total brain volume, white matter, and cortical gray matter in CHD; cortical gray matter and white matter reductions are at least 10% in HLHS from 30 weeks’ gestation, and postnatal pre-surgery cerebellar volume is reduced by 20% in SVP and TGA (n=19).
  • Acquired brain injury is common and often clinically silent; white matter injury is frequent, and preoperative injury is associated with lower cerebral blood flow, lower oxygen saturation, hypotension, and postnatal diagnosis, while follow-up after neonatal cardiac surgery remains short-term.

Methods

  • Narrative review integrating fetal and neonatal MRI studies—including diffusion MRI, phase-contrast MRI, and volumetric/cortical folding analyses—with cardiovascular physiology and neurodevelopmental outcome data in CHD.
  • Data include published fetal and neonatal cohorts and tables summarizing brain volumes/cortical folding and pre-/postoperative brain injury in SVP and TGA; no primary patient cohort or formal meta-analysis is reported.
  • Main analysis is qualitative synthesis linking altered cerebral perfusion and oxygen delivery to brain dysmaturation, acquired injury, and functional outcomes.

Limitations

  • Stated: data linking fetal/neonatal brain volumes to long-term neurodevelopmental outcome in critical CHD are lacking; no structural or functional network-based studies in fetal/neonatal CHD; follow-up after acquired brain injury around neonatal cardiac surgery is only short-term; substantial gaps remain in attributing outcomes to dysmaturation versus acquired injury.
  • Stated: white matter lesion scoring systems differ between research groups.
  • Evident: as a narrative review, it does not describe a systematic search strategy, formal risk-of-bias assessment, or quantitative synthesis.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1111/dmcn.13461

Cites

95 of 95 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 96 cited sources checked · 0 supported · 0 flagged

  • Premisecitation

    Advances in surgical technique and perioperative care in recent decades have raised survival among infants with even the most severe forms of congenital heart disease.

    “Improvements in surgical techniques and perioperative care over recent decades have led to an increase in survival of young infants with even the most critical forms of congenital heart disease (CHD). 1”
    Quote in the paperNot a substantial claim0 of 1 sources checked
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  • Interpretationreasoning

    In critical congenital heart disease, brain dysmaturation and acquired brain injury arise from both the underlying cardiovascular pathology and surgery performed during the neonatal period.

    “In critical CHD, brain dysmaturation and acquired brain injury result from a combination of underlying cardiovascular pathology and surgery performed in the neonatal period.”
    Quote in the paperSubstantial claim
  • Premisereasoning

    In left outflow tract obstruction such as hypoplastic left heart syndrome or aortic valve stenosis, the internal carotid arteries receive retrograde flow through the ductus arteriosus with blood of reduced oxygen saturation.

    “In conditions with left outflow tract obstruction (e.g.hypoplastic left heart syndrome [HLHS], aortic valve stenosis) the internal carotid arteries are supplied via retrograde flow via the ductus arteriosus (normally via antegrade flow from the left ventricle) with blood of reduced oxygen saturation (Fig. 1, HLHS).”
    Quote in the paperSubstantial claim
  • Premisecitation

    Reductions in executive performance are already present at school age in children with congenital heart disease.

    “Additionally, reductions in executive performance are already seen at this age.15”
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  • Premisecitation

    People who survive congenital heart disease continue to show functional deficits during early childhood and adolescence.

    “However, survivors of CHD continue to show functional deficits in early childhood and adolescence.[2][3][4][5]”
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  • May combine two claims. 29
  • Classified as probably not a substantial claim. 10

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    Premisecitation

    Childhood cognitive functioning declines as congenital heart disease severity increases, and it also appears to depend on the length of the neonatal perioperative course.

    “Childhood cognitive functioning decreases with increasing severity of CHD, 4 but also seems to be dependent on the length of neonatal perioperative course.16”
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    Interpretationreasoning

    MRI findings in infants with congenital heart disease can be used to assess potential clinical risk factors for brain abnormalities and to help predict functional outcomes early.

    “MRI findings in infants with CHD can be used to evaluate potential clinical risk factors for brain abnormalities, and aid prediction of functional outcomes at an early stage.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    At school age, motor developmental delays persist in children with all types of congenital heart disease, and IQ is lower than the population average.

    “At school age, motor developmental delays persist in children with all types of CHD 11 and IQs are lower than in the average population.[12][13][14]”
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    Premisecitation

    Adolescents with congenital heart disease have lower IQs and reduced executive functioning, shown by poorer perceptual reasoning and working memory than typically developing peers.

    “In adolescence, young people with CHD continue to show lower IQs, and reduced executive functioning can be recognized by the poorer perceptual reasoning and working memory scores in adolescents with CHD than their peers with typical development.[17][18][19]”
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  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    Information about when brain dysmaturation and acquired brain injury occur in congenital heart disease could be used to develop strategies that optimize neurodevelopment.

    “In addition, information on timing of brain dysmaturation and acquired brain injury in CHD has the potential to be used when developing strategies to optimize neurodevelopment.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Most studies find worse short- and long-term outcomes in patients with congenital heart disease than in healthy controls, and delays are more severe in single ventricle pathology than in biventricular defects.

    “Most studies report adverse short-and long-term outcomes in patients with CHD when compared with healthy controls, with more severe delays in single ventricle pathology (SVP) compared with biventricular cardiac defects.6”
    Quote in the paperSubstantial claim0 of 1 sources checked
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    Premisecitation

    In normal fetal circulation, about one quarter of ventricular output goes to the brain, and the brain accounts for half of total fetal oxygen consumption.

    “In the normal fetal circulation, around 25 per cent of the ventricular output will flow to the brain and the brain is responsible for 50 per cent of total fetal oxygen consumption.26”
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    Premisecitation

    In transposition of the great arteries, the aorta connects to the right ventricle, disrupting preferential streaming of oxygenated blood across the foramen ovale and lowering oxygen and nutrient delivery to the brain.

    “In transposition of the great arteries (TGA), the aorta is connected to the right ventricle, disrupting the normal preferential streaming of oxygenated blood across the foramen ovale (Fig. 1, TGA), resulting in lower oxygen and nutrient delivery to the brain.27”
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    Premisecitation

    Postnatal white matter fractional anisotropy is lower in infants with congenital heart disease who develop preoperative brain injury, supporting coexistence of white matter dysmaturation and acquired brain injury in early life.

    “Postnatal white matter fractional anisotropy is lower in infants with CHD who develop preoperative brain injury, 53 supporting the coexistence of white matter dysmaturation and acquired brain injury in early life.”
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    Premisecitation

    The basal ganglia and thalami are smaller in single ventricle pathology and transposition of the great arteries than in healthy controls, in both fetal and neonatal periods.

    “In addition, the basal ganglia and thalami are smaller in SVP and TGA when compared with healthy controls, in both the fetal 38 and neonatal 34 period.”
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    Premisecitation

    Brain microstructure is less disrupted in cases with a prenatal diagnosis, possibly because of earlier use of prostaglandin E1 to maintain the ductus arteriosus.

    “In contrast, brain microstructure is less disrupted in those cases with a prenatal diagnosis, which may result from earlier use of prostaglandin E1 (to maintain the ductus arteriosus).59”
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    Premisecitation

    Cortical gray matter and white matter volumes are reduced by at least 10% in hypoplastic left heart syndrome from the 30th week of gestation onward, and also in tetralogy of Fallot.

    “Cortical gray matter and white matter show reductions in volume of at least 10 per cent in HLHS from the 30th week of gestation onwards 38 but also in TOF.35”
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    Premisecitation

    Both single ventricle pathology and transposition of the great arteries had reduced oxygen delivery to the brain compared with coarctation of the aorta and healthy controls.

    “However, both SVP and TGA had reduced oxygen delivery to the brain compared with neonates with CoA and healthy controls.”
    Quote in the paperSubstantial claim0 of 1 sources checked
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    Interpretationcitation

    This 10% reduction in arterial oxygen saturation leads to a 15% reduction in cerebral oxygen delivery and a 32% reduction in cerebral oxygen consumption.

    “This reduction of arterial oxygen saturation leads to a 15 per cent reduction in cerebral oxygen delivery, and 32 per cent reduction in cerebral oxygen consumption.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Less complex sulci are already seen in fetuses with hypoplastic left heart syndrome around 30 weeks' gestation, and cortical folding is diminished in neonates with single ventricle pathology.

    “Less complex sulci (delayed first appearance or reduced depth) can already be seen in fetuses with HLHS around 30 weeks' gestation, 38 and cortical folding is diminished in neonates with SVP.38,39,42”
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    Interpretationcitation

    Chronic hypoxia likely makes brain development suboptimal, and decreased nutrient delivery such as glucose should also be considered a contributor to brain dysmaturation.

    “It is understandable that brain development will be suboptimal under conditions of chronic hypoxia, while decreased nutrient delivery (e.g.glucose) should also be considered as a contributor to brain dysmaturation.29”
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    Premisecitation

    Reduced oxygen delivery and oxygen consumption to the brain are associated with decreased total brain volume, and this is most severe in hypoplastic left heart syndrome compared with biventricular pathology.

    “Also, reduction in oxygen delivery and oxygen consumption to the brain is associated with decreased total brain volume, 28 which is most severe in HLHS when compared with biventricular pathology.”
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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    The most critical congenital heart defects require cardiac repair in the first weeks of life using cardiopulmonary bypass.

    “The most critical congenital heart defects require cardiac repair in the first weeks of life using cardiopulmonary bypass.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Lower fractional anisotropy values are associated with altered functional connectivity on electroencephalography before surgery in infants with congenital heart disease, highlighting synchronicity between structural and functional brain development.

    “The functional impact of early microstructural abnormalities identified on dMRI in infants with CHD has been highlighted recently in a study showing that lower fractional anisotropy values are associated with altered functional connectivity using electroencephalography before surgery, 60 highlighting the synchronicity between structural and functional brain development.”
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  • May combine two claims.

    Premisecitation

    All studies of fetal and neonatal brain volumes show significant reductions in total brain volume, white matter, and cortical gray matter in congenital heart disease compared with controls.

    “All studies of fetal and neonatal brain volumes (Table I) show significant reductions in total brain volume, white matter, and cortical gray matter (CGM) in CHD when compared with controls.28,30,33,34”
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  • May combine two claims.

    Interpretationreasoning

    Because blood flow was comparable, the reduced oxygen delivery in single ventricle pathology and transposition of the great arteries is mainly explained by lower arterial oxygen saturation: 98% in healthy controls, 98% in coarctation, 84% in single ventricle pathology, and 86% in transposition of the great arteries.

    “As blood flow was comparable, this is mainly explained by the decreased arterial oxygen saturation: 98% in healthy controls, 98% in coarctation, 84% in SVP, and 86% in TGA.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    In adolescents with cyanotic congenital heart disease, total brain volumes are significantly smaller than in healthy controls, and this decrease is strongly correlated with total IQ, verbal comprehension, perceptual reasoning, and working memory.

    “In adolescents with cyanotic CHD, total brain volumes are significantly smaller than in healthy controls, and this decrease is strongly correlated with total IQ, verbal comprehension, perceptual reasoning, and working memory.44”
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    Interpretationreasoning

    Such neuroprotective treatments could be advantageous for fetuses and neonates with critical congenital heart disease.

    “and might therefore benefit from these promising neuroprotective interventions.[92][93][94]”
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    • Rests on an assumption: The pathways targeted by neuroprotective drugs in other high-risk newborn groups (those with hypoxic-ischemic injury or stroke) are similar enough to those in fetuses and neonates with critical congenital heart disease that the same drugs might help CHD patients.

  • May combine two claims.

    Premisecitation

    Patients with single ventricle pathology have longer postoperative stay, more additional operations, and more frequent cardiopulmonary resuscitation and extracorporeal membrane oxygenation than patients with transposition of the great arteries, but incidences of acquired brain injury are similar between the two groups.

    “Patients with SVP show longer length of postoperative stay, more additional operations, more often cardiopulmonary resuscitation and extracorporal membrane oxygenation than patients with TGA, 82 but incidences of acquired brain injury are similar between the two groups.59,83”
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    Premisecitation

    Preoperative brain injury is accompanied by decreased microstructural white matter maturation, and fetal brain abnormalities are associated with increased risk of acquired brain injury after birth.

    “Preoperative brain injury is accompanied by decreased microstructural white matter maturation in several studies, 53,55,74 while fetal brain abnormalities are associated with an increased risk of acquired brain injury after birth.85”
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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    If several studies from a single centre reported similar findings for the same population, the review included only one of them.

    “When multiple studies from one centre showed similar results on the same population, only one of those studies was included.”
    Quote in the paperNot a substantial claim

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    Premisenone given

    After neonatal surgery with cardiopulmonary bypass, focal strokes of the basal ganglia and cortical gray matter may be observed, and these strokes are thought to have a thromboembolic origin.

    “After neonatal surgery with cardiopulmonary bypass, focal strokes of the basal ganglia and CGM may be observed (Table II), and these strokes are thought to have a thromboembolic origin.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The development of epilepsy after brain injury in the neonatal period is reported in various studies, but it normally responds well to drug therapy.

    “The development of epilepsy after brain injury in the neonatal period is reported in various studies, but normally responds well to drug therapy.90”
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    Premisecitation

    Lower preoperative oxygen saturation and preoperative hypotension are associated with increased risk of preoperative white matter injury, as is postnatal diagnosis of the heart defect.

    “Accordingly, lower preoperative oxygen saturation and preoperative hypotension are also associated with increased risk of preoperative WMI, 72,74,77,80 as is postnatal diagnosis of the heart defect.59”
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    Premisecitation

    There is a high incidence of acquired brain injury in neonates with congenital heart disease, and it is usually clinically silent, especially when sedation is given.

    “There is a high incidence of acquired brain injury in neonates with CHD (Table II), which is, in most cases, clinically silent (especially when sedation is given 69 ), highlighting the importance of neuroimaging to detect injury in this group.”
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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    To date, only short-term follow-up studies after acquired brain injury around neonatal cardiac surgery are reported.

    “To date, only short-term follow-up studies after acquired brain injury around neonatal cardiac surgery are reported.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The drugs may act beneficially on the pathways triggered by fetal or neonatal hypoxia.

    “These drugs might have a beneficial role in the pathways set in motion after fetal or neonatal hypoxia 91 and may reduce damage induced by reoxygenation and reperfusion of the brain.”
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    Premisecitation

    The drugs may lessen brain damage caused by reoxygenation and reperfusion.

    “These drugs might have a beneficial role in the pathways set in motion after fetal or neonatal hypoxia 91 and may reduce damage induced by reoxygenation and reperfusion of the brain.”
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    Premisenone given

    Clinical trials in other high-risk neonatal groups with hypoxic-ischemic injury or neonatal stroke are testing allopurinol, erythropoietin, xenon gas, and melatonin for protection and regeneration.

    “In other high-risk neonatal populations with hypoxic-ischemic injury or neonatal stroke, clinical trials are exploring the protective and regenerative role of several drugs: allopurinol, erythropoietin, xenon gas, and melatonin.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    Knowing when brain dysmaturation and acquired brain injury occur in congenital heart disease could inform strategies aimed at improving neurodevelopment.

    “Information on timing of brain dysmaturation and acquired brain injury in CHD can be used in the development of strategies to optimize neurodevelopment.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Critical congenital heart disease in fetuses and neonates involves both long-term hypoxia and sudden hypoxic-ischemic episodes.

    “Fetuses and neonates with critical CHD are experiencing both chronic hypoxia and acute hypoxic-ischemic events,”
    Quote in the paperSubstantial claim0 of 1 sources checked
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    Premisecitation

    Longer waiting times between birth and surgery are associated with higher rates of both pre- and postoperative brain injury, though reasons for postponement should be considered when interpreting this finding.

    “Longer waiting times between birth and surgery are associated with higher rates of both pre-and postoperative brain injury, although the reasons why surgery was postponed (postnatal diagnosis, haemodynamic instability) should be taken into account when interpreting this finding.80,84”
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    Premisecitation

    Involvement of the posterior limb of the internal capsule and cerebral peduncles on diffusion MRI is predictive of unilateral spastic cerebral palsy, which can already be present from 3 months of age.

    “Involvement of the posterior limb of the internal capsule and cerebral peduncles on dMRI is predictive of unilateral spastic cerebral palsy, which can already be present from 3 months of age onwards.87”
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38 of 38

  • The paper relies on this without support.

    The antenatal and neonatal periods are critical for optimal brain development, and the developing brain is especially vulnerable to haemodynamic disturbances during this time.

    “The antenatal and neonatal period are critical for optimal brain development; the developing brain is particularly vulnerable to haemodynamic disturbances during this time.”

  • The paper relies on this without support.

    Neonates have less autoregulatory capability and antioxidant scavenging capacity to cope with fluctuations in cerebral perfusion and oxygenation.

    “where neonates have less autoregulatory capability and antioxidant scavenging capacity to cope with such changes.”

  • The paper relies on this without support.

    The prognosis of acquired brain injury depends mainly on the location and extent of white matter injury and stroke.

    “The prognosis of acquired brain injury depends mainly on location and extent of WMI and stroke.”

  • The paper relies on this without support.

    The pathways targeted by neuroprotective drugs in other high-risk newborn groups (those with hypoxic-ischemic injury or stroke) are similar enough to those in fetuses and neonates with critical congenital heart disease that the same drugs might help CHD patients.

    “and might therefore benefit from these promising neuroprotective interventions.[92][93][94]”
4 of 4

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Authors
Claessens, N. H. P., Kelly, C. J., Counsell, S. J., & Benders, M. J. N. L.
Affiliations
  • University Medical Center Utrecht (NL)
  • King's College London (GB)
Corresponding author
Benders, Manon J N L
ORCID
Venue
Developmental Medicine & Child Neurology
Publisher
Wiley
Published
2017-05-19
Volume
59
Issue
9
Pages
894-902
ISSN
  • 0012-1622 (ISSN-L)
  • 1469-8749
DOI
10.1111/dmcn.13461
OpenAlex
W2615619116
Semantic Scholar
06a59e1fe2f76f4760660a48fa3f2b3983b0ea37
Cited by
59
References
95
Citations by year
2026: 4 · 2025: 5 · 2024: 6 · 2023: 8 · 2022: 4 · 2021: 10 · 2020: 8 · 2019: 9 · 2018: 5
FWCI
0.80
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Developmental Medicine & Child Neurology (publishedVersion)
  • PubMed (publishedVersion)
  • Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
  • Research Portal (King's College London) (submittedVersion, other-oa)
  • Utrecht University Repository (Utrecht University) (submittedVersion)
Funders
  • British Heart Foundation (FS/15/55/31649)
  • Royal De Heus
  • Medical Research Council (MR/L011530/1)
Topics
  • Health Sciences › Medicine › Epidemiology › Congenital Heart Disease Studies
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
Keywords
congenital heart disease, acquired brain injury, fetal MRI, neonatal MRI, cerebral perfusion, cerebral oxygen delivery, haemodynamic disturbances, brain development, functional outcome, neonatal surgery, neurological deficit
MeSH terms
Brain, Cardiovascular System, Heart Defects, Congenital, Humans, Infant, Neuroimaging

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