Impaired development of the cerebral cortex in infants with congenital heart disease is correlated to reduced cerebral oxygen delivery

Christopher J Kelly; Antonios Makropoulos; Lucilio Cordero-Grande; Jana Hutter; Anthony Price; Emer Hughes; Maria Murgasova; Rui Pedro A G Teixeira; Johannes K Steinweg; Sagar Kulkarni; Loay Rahman; Hui Zhang; Daniel C Alexander; Kuberan Pushparajah; Daniel Rueckert; Joseph V Hajnal; John Simpson; A David Edwards; Mary A Rutherford; Serena J Counsell

doi:10.1038/s41598-017-14939-z

Impaired development of the cerebral cortex in infants with congenital heart disease is correlated to reduced cerebral oxygen delivery

Christopher J Kelly, Antonios Makropoulos, Lucilio Cordero-Grande, Jana Hutter, Anthony Price, Emer Hughes, Maria Murgasova, Rui Pedro A G Teixeira, Johannes K Steinweg, Sagar Kulkarni, Loay Rahman, Hui Zhang, Daniel C Alexander, Kuberan Pushparajah, Daniel Rueckert, Joseph V Hajnal, John Simpson, A David Edwards, Mary A Rutherford, Serena J Counsell

Centre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King's College London, King's Health Partners, St. Thomas' HospitalLondon, United Kingdom.
Imperial College London
UCL University College London
Evelina London Children's Hospital
Centre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King's College London, London, United Kingdom. [email protected].

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Abstract

Neurodevelopmental impairment is the most common comorbidity associated with complex congenital heart disease (CHD), while the underlying biological mechanism remains unclear. We hypothesised that impaired cerebral oxygen delivery in infants with CHD is a cause of impaired cortical development, and predicted that cardiac lesions most associated with reduced cerebral oxygen delivery would demonstrate the greatest impairment of cortical development. We compared 30 newborns with complex CHD prior to surgery and 30 age-matched healthy controls using brain MRI. The cortex was assessed using high resolution, motion-corrected T2-weighted images in natural sleep, analysed using an automated pipeline. Cerebral oxygen delivery was calculated using phase contrast angiography and pre-ductal pulse oximetry, while regional cerebral oxygen saturation was estimated using near-infrared spectroscopy. We found that impaired cortical grey matter volume and gyrification index in newborns with complex CHD was linearly related to reduced cerebral oxygen delivery, and that cardiac lesions associated with the lowest cerebral oxygen delivery were associated with the greatest impairment of cortical development. These findings suggest that strategies to improve cerebral oxygen delivery may help reduce brain dysmaturation in newborns with CHD, and may be most relevant for children with CHD whose cardiac defects remain unrepaired for prolonged periods after birth.

Original language	English
Pages (from-to)	15088
Journal	Scientific Reports
Volume	7
Issue number	1
DOIs	https://doi.org/10.1038/s41598-017-14939-z
Publication status	Published - 8 Nov 2017

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Journal Article

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Impaired development of the_KELLY_Publishedonline8November2017_GOLD VoR (CC BYFinal published version, 1.98 MB

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Kelly, C. J., Makropoulos, A., Cordero-Grande, L., Hutter, J., Price, A., Hughes, E., Murgasova, M., Teixeira, R. P. A. G., Steinweg, J. K., Kulkarni, S., Rahman, L., Zhang, H., Alexander, D. C., Pushparajah, K., Rueckert, D., Hajnal, J. V., Simpson, J., Edwards, A. D., Rutherford, M. A., & Counsell, S. J. (2017). Impaired development of the cerebral cortex in infants with congenital heart disease is correlated to reduced cerebral oxygen delivery. Scientific Reports, 7(1), 15088. https://doi.org/10.1038/s41598-017-14939-z

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abstract = "Neurodevelopmental impairment is the most common comorbidity associated with complex congenital heart disease (CHD), while the underlying biological mechanism remains unclear. We hypothesised that impaired cerebral oxygen delivery in infants with CHD is a cause of impaired cortical development, and predicted that cardiac lesions most associated with reduced cerebral oxygen delivery would demonstrate the greatest impairment of cortical development. We compared 30 newborns with complex CHD prior to surgery and 30 age-matched healthy controls using brain MRI. The cortex was assessed using high resolution, motion-corrected T2-weighted images in natural sleep, analysed using an automated pipeline. Cerebral oxygen delivery was calculated using phase contrast angiography and pre-ductal pulse oximetry, while regional cerebral oxygen saturation was estimated using near-infrared spectroscopy. We found that impaired cortical grey matter volume and gyrification index in newborns with complex CHD was linearly related to reduced cerebral oxygen delivery, and that cardiac lesions associated with the lowest cerebral oxygen delivery were associated with the greatest impairment of cortical development. These findings suggest that strategies to improve cerebral oxygen delivery may help reduce brain dysmaturation in newborns with CHD, and may be most relevant for children with CHD whose cardiac defects remain unrepaired for prolonged periods after birth.",

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Kelly, CJ, Makropoulos, A, Cordero-Grande, L , Hutter, J , Price, A, Hughes, E, Murgasova, M , Teixeira, RPAG , Steinweg, JK, Kulkarni, S, Rahman, L, Zhang, H, Alexander, DC, Pushparajah, K, Rueckert, D, Hajnal, JV, Simpson, J, Edwards, AD , Rutherford, MA & Counsell, SJ 2017, 'Impaired development of the cerebral cortex in infants with congenital heart disease is correlated to reduced cerebral oxygen delivery', Scientific Reports, vol. 7, no. 1, pp. 15088. https://doi.org/10.1038/s41598-017-14939-z

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AU - Kelly, Christopher J

AU - Makropoulos, Antonios

AU - Cordero-Grande, Lucilio

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AU - Price, Anthony

AU - Hughes, Emer

AU - Murgasova, Maria

AU - Teixeira, Rui Pedro A G

AU - Steinweg, Johannes K

AU - Kulkarni, Sagar

AU - Rahman, Loay

AU - Zhang, Hui

AU - Alexander, Daniel C

AU - Pushparajah, Kuberan

AU - Rueckert, Daniel

AU - Hajnal, Joseph V

AU - Simpson, John

AU - Edwards, A David

AU - Rutherford, Mary A

AU - Counsell, Serena J

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N2 - Neurodevelopmental impairment is the most common comorbidity associated with complex congenital heart disease (CHD), while the underlying biological mechanism remains unclear. We hypothesised that impaired cerebral oxygen delivery in infants with CHD is a cause of impaired cortical development, and predicted that cardiac lesions most associated with reduced cerebral oxygen delivery would demonstrate the greatest impairment of cortical development. We compared 30 newborns with complex CHD prior to surgery and 30 age-matched healthy controls using brain MRI. The cortex was assessed using high resolution, motion-corrected T2-weighted images in natural sleep, analysed using an automated pipeline. Cerebral oxygen delivery was calculated using phase contrast angiography and pre-ductal pulse oximetry, while regional cerebral oxygen saturation was estimated using near-infrared spectroscopy. We found that impaired cortical grey matter volume and gyrification index in newborns with complex CHD was linearly related to reduced cerebral oxygen delivery, and that cardiac lesions associated with the lowest cerebral oxygen delivery were associated with the greatest impairment of cortical development. These findings suggest that strategies to improve cerebral oxygen delivery may help reduce brain dysmaturation in newborns with CHD, and may be most relevant for children with CHD whose cardiac defects remain unrepaired for prolonged periods after birth.

AB - Neurodevelopmental impairment is the most common comorbidity associated with complex congenital heart disease (CHD), while the underlying biological mechanism remains unclear. We hypothesised that impaired cerebral oxygen delivery in infants with CHD is a cause of impaired cortical development, and predicted that cardiac lesions most associated with reduced cerebral oxygen delivery would demonstrate the greatest impairment of cortical development. We compared 30 newborns with complex CHD prior to surgery and 30 age-matched healthy controls using brain MRI. The cortex was assessed using high resolution, motion-corrected T2-weighted images in natural sleep, analysed using an automated pipeline. Cerebral oxygen delivery was calculated using phase contrast angiography and pre-ductal pulse oximetry, while regional cerebral oxygen saturation was estimated using near-infrared spectroscopy. We found that impaired cortical grey matter volume and gyrification index in newborns with complex CHD was linearly related to reduced cerebral oxygen delivery, and that cardiac lesions associated with the lowest cerebral oxygen delivery were associated with the greatest impairment of cortical development. These findings suggest that strategies to improve cerebral oxygen delivery may help reduce brain dysmaturation in newborns with CHD, and may be most relevant for children with CHD whose cardiac defects remain unrepaired for prolonged periods after birth.

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SN - 2045-2322

VL - 7

SP - 15088

JO - Scientific Reports

JF - Scientific Reports

IS - 1

ER -

Impaired development of the cerebral cortex in infants with congenital heart disease is correlated to reduced cerebral oxygen delivery

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