Abnormal Microstructural Development of the Cerebral Cortex in Neonates With Congenital Heart Disease Is Associated With Impaired Cerebral Oxygen Delivery.

Publisher: Wiley-Blackwell Country of Publication: England NLM ID: 101580524 Publication Model: Print Cited Medium: Internet ISSN: 2047-9980 (Electronic) Linking ISSN: 20479980 NLM ISO Abbreviation: J Am Heart Assoc Subsets: MEDLINE

Original Publication: Oxford : Wiley-Blackwell

Cerebrovascular Circulation* ; Diffusion Magnetic Resonance Imaging*; Brain Diseases/*diagnostic imaging ; Cerebral Cortex/*blood supply ; Cerebral Cortex/*diagnostic imaging ; Heart Defects, Congenital/*complications ; Hypoxia/*etiology ; Oxygen/*blood; Age Factors ; Biomarkers/blood ; Brain Diseases/blood ; Brain Diseases/etiology ; Brain Diseases/physiopathology ; Case-Control Studies ; Cerebral Cortex/growth & development ; Child Development ; Female ; Heart Defects, Congenital/blood ; Heart Defects, Congenital/diagnostic imaging ; Heart Defects, Congenital/physiopathology ; Humans ; Hypoxia/blood ; Hypoxia/diagnosis ; Hypoxia/physiopathology ; Infant, Newborn ; Male ; Oximetry ; Predictive Value of Tests ; Prospective Studies

Background Abnormal macrostructural development of the cerebral cortex has been associated with hypoxia in infants with congenital heart disease ( CHD ). Animal studies have suggested that hypoxia results in cortical dysmaturation at the cellular level. New magnetic resonance imaging techniques offer the potential to investigate the relationship between cerebral oxygen delivery and cortical microstructural development in newborn infants with CHD . Methods and Results We measured cortical macrostructural and microstructural properties in 48 newborn infants with serious or critical CHD and 48 age-matched healthy controls. Cortical volume and gyrification index were calculated from high-resolution structural magnetic resonance imaging. Neurite density and orientation dispersion indices were modeled using high-angular-resolution diffusion magnetic resonance imaging. Cerebral oxygen delivery was estimated in infants with CHD using phase contrast magnetic resonance imaging and preductal pulse oximetry. We used gray matter-based spatial statistics to examine voxel-wise group differences in cortical microstructure. Microstructural development of the cortex was abnormal in 48 infants with CHD , with regions of increased fractional anisotropy and reduced orientation dispersion index compared with 48 healthy controls, correcting for gestational age at birth and scan (family-wise error corrected for multiple comparisons at P<0.05). Regions of reduced cortical orientation dispersion index in infants with CHD were related to impaired cerebral oxygen delivery ( R ² =0.637; n=39). Cortical orientation dispersion index was associated with the gyrification index ( R ² =0.589; P<0.001; n=48). Conclusions This study suggests that the primary component of cerebral cortex dysmaturation in CHD is impaired dendritic arborization, which may underlie abnormal macrostructural findings reported in this population, and that the degree of impairment is related to reduced cerebral oxygen delivery.

J Am Heart Assoc. 2019 Mar 5;8(5):e009893. (PMID: 30821171)
J Comp Neurol. 1988 May 15;271(3):355-86. (PMID: 2454966)
Neuroimage. 2016 Nov 15;142:394-406. (PMID: 27523449)
Neuroimage. 2006 Jul 15;31(4):1487-505. (PMID: 16624579)
Neuroimage. 2012 Jul 16;61(4):1000-16. (PMID: 22484410)
Magn Reson Med. 2018 Mar;79(3):1276-1292. (PMID: 28557055)
Cereb Cortex. 1995 Jan-Feb;5(1):56-63. (PMID: 7719130)
Cereb Cortex. 2003 Jun;13(6):541-9. (PMID: 12764027)
Cereb Cortex. 2017 Jul 1;27(7):3736-3751. (PMID: 27600849)
Ann Clin Transl Neurol. 2017 Aug 15;4(9):663-679. (PMID: 28904988)
Cereb Cortex. 2013 Dec;23(12):2932-43. (PMID: 22977063)
Circulation. 2016 Feb 9;133(6):566-75. (PMID: 26769743)
Med Image Anal. 2012 Dec;16(8):1550-64. (PMID: 22939612)
Neuroimage. 2009 Jan 1;44(1):83-98. (PMID: 18501637)
J Thorac Cardiovasc Surg. 2004 Dec;128(6):841-9. (PMID: 15573068)
Proc Natl Acad Sci U S A. 2013 Jun 4;110(23):9541-6. (PMID: 23696665)
Pediatr Res. 2016 Aug;80(2):172-7. (PMID: 27055190)
Epilepsy Res. 2014 Feb;108(2):336-9. (PMID: 24315018)
Circulation. 2010 Jan 5;121(1):26-33. (PMID: 20026783)
J Thorac Cardiovasc Surg. 2009 Mar;137(3):529-36; discussion 536-7. (PMID: 19258059)
Neuroimage. 2010 Nov 1;53(2):450-9. (PMID: 20630489)
Pediatrics. 1990 Jun;85(6):984-90. (PMID: 2339047)
Ultrasound Obstet Gynecol. 2015 Aug;46(2):174-81. (PMID: 25270670)
Neuroimage. 2015 Feb 15;107:242-256. (PMID: 25498427)
Sci Transl Med. 2013 Jan 16;5(168):168ra7. (PMID: 23325800)
Neuroimage. 2016 Jan 15;125:456-478. (PMID: 26499811)
NMR Biomed. 2012 Sep;25(9):1063-72. (PMID: 22290659)
Med Image Anal. 2001 Jun;5(2):143-56. (PMID: 11516708)
Hum Brain Mapp. 2002 Nov;17(3):143-55. (PMID: 12391568)
Neuroimage. 2003 Oct;20(2):870-88. (PMID: 14568458)
Nat Rev Cardiol. 2011 Jan;8(1):50-60. (PMID: 21045784)
AJNR Am J Neuroradiol. 1996 Aug;17(7):1303-11. (PMID: 8871716)
J Thorac Cardiovasc Surg. 2016 Oct;152(4):1095-103. (PMID: 27349283)
J Neurosci. 2017 Feb 22;37(8):1971-1983. (PMID: 28069920)
Magn Reson Med. 2018 Mar;79(3):1365-1376. (PMID: 28626962)
Pediatrics. 1990 Jun;85(6):991-1000. (PMID: 2339048)
Acad Radiol. 2008 Nov;15(11):1360-75. (PMID: 18995188)
Lancet. 2011 Aug 27;378(9793):785-94. (PMID: 21820732)
Ann Neurol. 1989 Feb;25(2):196-9. (PMID: 2919869)
Circulation. 2012 Aug 28;126(9):1143-72. (PMID: 22851541)
Circulation. 2011 Sep 20;124(12):1361-9. (PMID: 21875911)
IEEE Trans Med Imaging. 2019 Mar;38(3):834-843. (PMID: 30296214)
Neuroimage. 2018 Jun;173:88-112. (PMID: 29409960)
Circulation. 2002 Sep 24;106(12 Suppl 1):I109-14. (PMID: 12354718)
J Pediatr. 2013 Nov;163(5):1507-10. (PMID: 23988135)
Circulation. 2015 Apr 14;131(15):1313-23. (PMID: 25762062)
Sci Rep. 2017 Nov 8;7(1):15088. (PMID: 29118365)
Pediatrics. 2017 Jul;140(1):. (PMID: 28607205)
Neuroimage. 2005 Sep;27(3):579-86. (PMID: 15921934)
J Thorac Cardiovasc Surg. 2012 Jun;143(6):1264-70. (PMID: 22143100)
Magn Reson Med. 2017 Aug;78(2):794-804. (PMID: 27643791)
Pediatr Res. 2016 Nov;80(5):668-674. (PMID: 27434120)
Magn Reson Med. 2016 Nov;76(5):1574-1581. (PMID: 26745823)
Neuroimage. 2014 Aug 1;96:288-99. (PMID: 24680870)
Circ Res. 2017 Mar 17;120(6):923-940. (PMID: 28302740)
Radiology. 1996 Aug;200(2):389-96. (PMID: 8685331)
Cereb Cortex. 2002 Dec;12(12):1237-43. (PMID: 12427675)
Neuroimage. 2006 Jul 1;31(3):1116-28. (PMID: 16545965)
Nat Rev Neurosci. 2008 Feb;9(2):110-22. (PMID: 18209730)
Neuroimage. 2015 May 1;111:580-9. (PMID: 25681570)
Sci Transl Med. 2017 Jan 25;9(374):. (PMID: 28123074)
IEEE Trans Med Imaging. 2014 Sep;33(9):1818-31. (PMID: 24816548)
Neuroimage. 2019 Jan 15;185:764-775. (PMID: 29802969)

WT 203148/Z/16/Z United Kingdom WT_ Wellcome Trust; United Kingdom DH_ Department of Health; MR/K006355/1 United Kingdom MRC_ Medical Research Council; MC_U120088465 United Kingdom MRC_ Medical Research Council; MR/L011530/1 United Kingdom MRC_ Medical Research Council; MR/N026063/1 United Kingdom MRC_ Medical Research Council; FS/15/55/31649 United Kingdom BHF_ British Heart Foundation

Keywords: brain imaging; cerebral blood flow; congenital heart disease; development; magnetic resonance imaging

0 (Biomarkers)
S88TT14065 (Oxygen)

Date Created: 20190302 Date Completed: 20200714 Latest Revision: 20210109

20240829

PMC6474935

10.1161/JAHA.118.009893

30821171