Selective Vulnerability in the Developing Brain in Fetuses with Congenital Heart Disease
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1 4 th Annual Cardiac Neurodevelopmental Symposium Selective Vulnerability in the Developing Brain in Fetuses with Congenital Heart Disease Catherine Limperopoulos, PhD
2 Brain Injury and Congenital Heart Disease (CHD) Diagnostic and surgical advances have greatly enhanced survival Brain injury is a major complication of CHD Growing population of survivors with neurologic dysfunction New profile of neurologic dysfunction
3 Periods of Risk for Brain Injury in CHD Next Era - Early detection of brain injury in the fetus Fetal Pre-operative Intra-operative Post-operative
4 Mechanisms of Fetal Brain Maldevelopment Genetic conditions Epigenetic/programming mechanisms Fetal insults Cerebral disruptions Acquired encephaloclastic lesions (e.g., cerebrovascular insults)
5 Critical Periods of Normal Brain Development Myelination Organization Neuronal migration Neuronal proliferation Prosencephalic development Primary neurulation Months
6 Normal Third Trimester Brain Development **3T high energy dependent processes vulnerable to conditions that restrict cerebral oxygen/substrate supply 6
7 Structural Evidence for Impaired Brain Development of Fetal Onset
8 Conventional brain MRI in Fetuses with CHD Retrospective review of 53 cases (Mlczoch, 2012) 39% abnormal fetal brain MRI (malformations/acquired) Malformations 33% Acquired lesions 24% Abnormal CSF spaces 43% Prospective review of 144 CHD cases vs 194 controls (Brossard-Racine, 2014) 23% abnormal fetal brain MRI vs 1.5 controls (p<0.001) Malformations/acquired lesions Mild unilateral ventriculomegaly Increased extra-axial spaces Immature brain appearance (underdevelopment of fissures/sulci for GA) Periventricular cysts / WM signal hyperintensities Inferior vermian hypoplasia
9 Conventional Fetal-Neonatal Neuroimaging Conventional brain imaging only identifies the tip of the iceberg
10 Fetal Brain Tissue Quantification
11 Brain Growth in Fetuses with CHD and Controls p<0.001 Control CHD Limperopoulos et al., Circulation 2010
12 Fetal Brain Tissue Growth in HLHS p<0.001 Clouchoux et al., Cerebral Cortex, 2013
13 Cortical Development in the Fetus 27 wks 33 wks High-resolution reconstructed brain and inner cortical surface Feature extraction Probability map of sulci location Average sulcal depth between 25 and 35 weeks GA Clouchoux et al., 2012
14 Fetal Gyrification/Surface Area in HLHS vs. Controls p<0.001
15 Differences in Cortical Depth in HLHS vs. Controls Clouchoux et al., Cerebral Cortex, 2013
16 Fetal Brain Oxygenation and Brain Growth Sun et al., Circulation, 2015
17 Fetal Brain Metabolism Cho Cr/PCr NAA Lac Cho turn-over marker of cell membranes, Cr/PCr energy metabolism NAA neuronal marker, Lac end product of anaerobic glycolysis
18 Metabolic Profiles in CHD vs. Control Fetuses Control Fetuses CHD Fetuses
19 Relationship Between Aortic Arch Flow & NAA Limperopoulos et al., Circulation, 2010
20 Amplitude Cerebral Lactate in Fetuses with CHD No control fetus had detectable cerebral lactate Cerebral lactate was present in 24% CHD fetuses Cho Cr NA A Lac Frequency (ppm)
21 Total Brain Volume, NAA:Cho, and Lactate in Fetal CHD
22 Predictive Value of Quantitative Fetal MRI 18 month follow up: N=94 16 died Fetal lactate associated with fetal demise/preoperative death (p<0.01) Total brain volume associated with MDI & PDI (p=0.01) Total brain volume associated with maladaptive behaviors (p=0.02)
23 Summary Impaired brain growth and metabolism can be detected early 3 rd T in CHD fetus Local cortical folding delays are present as early as 25 weeks and appear to precede volumetric growth disturbances Fetal lactate is predictive of fetal / neonatal death Reduced fetal brain volume is associated with long-term developmental delays These data support a fetal onset of mechanisms leading to neurodevelopmental disabilities in children with CHD 23
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