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Research ArticlePEDIATRICS

Brain and CSF Volumes in Fetuses and Neonates with Antenatal Diagnosis of Critical Congenital Heart Disease: A Longitudinal MRI Study

N.H.P. Claessens, N. Khalili, I. Isgum, H. ter Heide, T.J. Steenhuis, E. Turk, N.J.G. Jansen, L.S. de Vries, J.M.P.J. Breur, R. de Heus and M.J.N.L. Benders
American Journal of Neuroradiology March 2019, DOI: https://doi.org/10.3174/ajnr.A6021
N.H.P. Claessens
aFrom the Departments of Neonatology (N.H.P.C., E.T., L.S.d.V., M.J.N.L.B.)
bPediatric Cardiology (N.H.P.C., H.t.H., T.J.S., J.M.P.J.B.)
cPediatric Intensive Care (N.H.P.C., N.J.G.J.)
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  • ORCID record for N.H.P. Claessens
N. Khalili
eImage Sciences Institute (N.K., I.I.), University Medical Center Utrecht, Utrecht, the Netherlands
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  • ORCID record for N. Khalili
I. Isgum
eImage Sciences Institute (N.K., I.I.), University Medical Center Utrecht, Utrecht, the Netherlands
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H. ter Heide
bPediatric Cardiology (N.H.P.C., H.t.H., T.J.S., J.M.P.J.B.)
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T.J. Steenhuis
bPediatric Cardiology (N.H.P.C., H.t.H., T.J.S., J.M.P.J.B.)
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E. Turk
aFrom the Departments of Neonatology (N.H.P.C., E.T., L.S.d.V., M.J.N.L.B.)
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N.J.G. Jansen
cPediatric Intensive Care (N.H.P.C., N.J.G.J.)
fDepartment of Pediatrics (N.J.G.J.), Beatrix Children's Hospital, University Medical Center Groningen, Groningen, the Netherlands.
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L.S. de Vries
aFrom the Departments of Neonatology (N.H.P.C., E.T., L.S.d.V., M.J.N.L.B.)
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J.M.P.J. Breur
bPediatric Cardiology (N.H.P.C., H.t.H., T.J.S., J.M.P.J.B.)
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R. de Heus
dObstetrics (R.d.H.), Wilhelmina Children's Hospital, Utrecht, the Netherlands
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M.J.N.L. Benders
aFrom the Departments of Neonatology (N.H.P.C., E.T., L.S.d.V., M.J.N.L.B.)
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Abstract

BACKGROUND AND PURPOSE: Fetuses and neonates with critical congenital heart disease are at risk of delayed brain development and neurodevelopmental impairments. Our aim was to investigate the association between fetal and neonatal brain volumes and neonatal brain injury in a longitudinally scanned cohort with an antenatal diagnosis of critical congenital heart disease and to relate fetal and neonatal brain volumes to postmenstrual age and type of congenital heart disease.

MATERIALS AND METHODS: This was a prospective, longitudinal study including 61 neonates with critical congenital heart disease undergoing surgery with cardiopulmonary bypass <30 days after birth and MR imaging of the brain; antenatally (33 weeks postmenstrual age), neonatal preoperatively (first week), and postoperatively (7 days postoperatively). Twenty-six had 3 MR imaging scans; 61 had at least 1 fetal and/or neonatal MR imaging scan. Volumes (cubic centimeters) were calculated for total brain volume, unmyelinated white matter, cortical gray matter, cerebellum, extracerebral CSF, and ventricular CSF. MR images were reviewed for ischemic brain injury.

RESULTS: Total fetal brain volume, cortical gray matter, and unmyelinated white matter positively correlated with preoperative neonatal total brain volume, cortical gray matter, and unmyelinated white matter (r = 0.5–0.58); fetal ventricular CSF and extracerebral CSF correlated with neonatal ventricular CSF and extracerebral CSF (r = 0.64 and 0.82). Fetal cortical gray matter, unmyelinated white matter, and the cerebellum were negatively correlated with neonatal ischemic injury (r = −0.46 to −0.41); fetal extracerebral CSF and ventricular CSF were positively correlated with neonatal ischemic injury (r = 0.40 and 0.23). Unmyelinated white matter:total brain volume ratio decreased with increasing postmenstrual age, with a parallel increase of cortical gray matter:total brain volume and cerebellum:total brain volume. Fetal ventricular CSF:intracranial volume and extracerebral CSF:intracranial volume ratios decreased with increasing postmenstrual age; however, neonatal ventricular CSF:intracranial volume and extracerebral CSF:intracranial volume ratios increased with postmenstrual age.

CONCLUSIONS: This study reveals that fetal brain volumes relate to neonatal brain volumes in critical congenital heart disease, with a negative correlation between fetal brain volumes and neonatal ischemic injury. Fetal brain imaging has the potential to provide early neurologic biomarkers.

ABBREVIATIONS:

CGM
cortical gray matter
CHD
congenital heart disease
ECSF
extracerebral CSF
ICV
intracranial volume
PMA
postmenstrual age
TBV
total brain volume
UWM
unmyelinated white matter
VCSF
ventricular CSF
WMI
white matter injury

Footnotes

  • Roel de Heus and Manon J.N.L. Benders share last authorship.

  • Disclosures: Ivana Isgum—UNRELATED: Grants/Grants Pending: research grant funded by Nutricia Research, University Medical Center Utrecht, Utrecht University*; Patents (Planned, Pending or Issued): I am an inventor of 1 accepted and 1 pending patent; Stock/Stock Options: I am a scientific founder and shareholder of Quantib-U B.V.; Linda S. de Vries—UNRELATED: Employment: Consultant Neonatologist at UMCU*; Grants/Grants Pending: ZonMw grant for neonatal stroke*; Payment for Lectures Including Service on Speakers Bureaus: yearly ultrasound course in London, Imperial College, sometimes honorarium for giving a lecture*; Royalties: 3 books: Hellström-Westas L, de Vries LS, Rosen I. An Atlas of Amplitude-Integrated EEGs in The Newborn. 2nd ed, Informa Health, London, August 2008; Govaert P, de Vries LS. An Atlas of Neonatal Brain Sonography, 2nd ed (CDM 182–183), Mac Keith Press, ISBN: 978-1-898683-56-8, July 2010; Volpe's Textbook Neurology of the Newborn, Elsevier, 2017.* *Money paid to the Institution.

  • © 2019 by American Journal of Neuroradiology
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Brain and CSF Volumes in Fetuses and Neonates with Antenatal Diagnosis of Critical Congenital Heart Disease: A Longitudinal MRI Study
N.H.P. Claessens, N. Khalili, I. Isgum, H. ter Heide, T.J. Steenhuis, E. Turk, N.J.G. Jansen, L.S. de Vries, J.M.P.J. Breur, R. de Heus, M.J.N.L. Benders
American Journal of Neuroradiology Mar 2019, DOI: 10.3174/ajnr.A6021

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Brain and CSF Volumes in Fetuses and Neonates with Antenatal Diagnosis of Critical Congenital Heart Disease: A Longitudinal MRI Study
N.H.P. Claessens, N. Khalili, I. Isgum, H. ter Heide, T.J. Steenhuis, E. Turk, N.J.G. Jansen, L.S. de Vries, J.M.P.J. Breur, R. de Heus, M.J.N.L. Benders
American Journal of Neuroradiology Mar 2019, DOI: 10.3174/ajnr.A6021
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