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Neuroimaging and Neurodevelopmental Outcomes Among Individuals With Complex Congenital Heart Disease: JACC State-of-the-Art ReviewGET ACCESS

JACC State-of-the-Art Review

J Am Coll Cardiol, 82 (23) 2225–2245
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Abstract

Although neuroimaging advances have deepened our understanding of brain health in individuals with congenital heart disease (CHD), it is less clear how neuroimaging findings relate to neurodevelopmental and mental health outcomes across the lifespan. We systematically synthesized and critically evaluated evidence on associations between neuroimaging and neurodevelopmental, neurocognitive, psychiatric, or behavioral outcomes among individuals with transposition of great arteries or single-ventricle CHD (Protocol CRD42021229617). Six databases were searched and 45 papers from 25 unique studies were identified. Structural brain injury was generally linked to poorer neurodevelopment in infancy. Brain volumes and microstructural and functional brain changes appear linked to neurocognitive outcomes, including deficits in attention, learning, memory, and executive function in children and adolescents. Fetal neuroimaging studies were limited. Four papers investigated psychiatric outcomes; none found associations with neuroimaging. Multicenter, longitudinal studies incorporating functional neuroimaging and mental health outcomes are much-needed to inform early neuroprotective and therapeutic strategies in CHD.

Highlights

Advances in neuroimaging have improved understanding of brain health and development in patients with CHD.

Structural, microstructural, and functional neuroimaging findings are linked to neurocognitive outcomes across the lifespan in patients with CHD.

Multicenter, longitudinal studies incorporating mental health metrics are needed to inform neuroprotective and therapeutic strategies in patients with CHD.

References

  • 1. Khairy P., Ionescu-Ittu R., Mackie A.S., Abrahamowicz M., Pilote L., Marelli A.J. "Changing mortality in congenital heart disease". J Am Coll Cardiol . 2010;56:1149-1157.

    View ArticleGoogle Scholar
  • 2. Kalfa D., Kasmi L., Geronikola N., et al. "Cognitive outcomes and health-related quality of life in adults two decades after the arterial switch operation for transposition of the great arteries". J Thorac Cardiovasc Surg . 2017;154:1028-1035.

    CrossrefMedlineGoogle Scholar
  • 3. Bolduc M.-E., Dionne E., Gagnon I., Rennick J.E., Majnemer A., Brossard-Racine M. "Motor impairment in children with congenital heart defects: a systematic review". Pediatrics . 2020;146:e20200083.

    CrossrefMedlineGoogle Scholar
  • 4. Sprong M.C., Broeders W., van der Net J., et al. "Motor developmental delay after cardiac surgery in children with a critical congenital heart defect: a systematic literature review and meta-analysis". Pediatr Phys Ther . 2021;33:186-197.

    CrossrefMedlineGoogle Scholar
  • 5. Huisenga D., La Bastide-Van Gemert S., Van Bergen A., Sweeney J., Hadders-Algra M. "Developmental outcomes after early surgery for complex congenital heart disease: a systematic review and meta-analysis". Dev Med Child Neurol . 2021;63:29-46.

    CrossrefMedlineGoogle Scholar
  • 6. Mebius M.J., Kooi E.M., Bilardo C.M., Bos A.F. "Brain injury and neurodevelopmental outcome in congenital heart disease: a systematic review". Pediatrics . 2017;140:e20164055.

    CrossrefMedlineGoogle Scholar
  • 7. Mills R., McCusker C.G., Tennyson C., Hanna D. "Neuropsychological outcomes in CHD beyond childhood: a meta-analysis". Cardiol Young . 2018;28:421-431.

    CrossrefMedlineGoogle Scholar
  • 8. Bellinger D.C., Wypij D., Rivkin M.J., et al. "Adolescents with d-transposition of the great arteries corrected with the arterial switch procedure: neuropsychological assessment and structural brain imaging". Circulation . 2011;124:1361-1369.

    CrossrefMedlineGoogle Scholar
  • 9. Feldmann M., Bataillard C., Ehrler M., et al. "Cognitive and executive function in congenital heart disease: a meta-analysis". Pediatrics . 2021;148:e2021050875.

    CrossrefMedlineGoogle Scholar
  • 10. Sanz J.H., Berl M.M., Armour A.C., Wang J., Cheng Y.I., Donofrio M.T. "Prevalence and pattern of executive dysfunction in school age children with congenital heart disease". Congenit Heart Dis . 2017;12:202-209.

    CrossrefMedlineGoogle Scholar
  • 11. Cassidy A.R., White M.T., DeMaso D.R., Newburger J.W., Bellinger D.C. "Processing speed, executive function, and academic achievement in children with dextro-transposition of the great arteries: testing a longitudinal developmental cascade model". Neuropsychology . 2016;30:874-885.

    CrossrefMedlineGoogle Scholar
  • 12. Marelli A., Miller S.P., Marino B.S., Jefferson A.L., Newburger J.W. "Brain in congenital heart disease across the lifespan: the cumulative burden of injury". Circulation . 2016;133:1951-1962.

    CrossrefMedlineGoogle Scholar
  • 13. Carey A.S., Liang L., Edwards J., et al. "Effect of copy number variants on outcomes for infants with single ventricle heart defects". Circ Cardiovasc Genet . 2013;6:444-451.

    CrossrefMedlineGoogle Scholar
  • 14. Gaynor J.W., Stopp C., Wypij D., et al. "Neurodevelopmental outcomes after cardiac surgery in infancy". Pediatrics . 2015;135:816-825.

    CrossrefMedlineGoogle Scholar
  • 15. Gaynor J.W., Stopp C., Wypij D., et al. "Impact of operative and postoperative factors on neurodevelopmental outcomes after cardiac operations". Ann Thorac Surg . 2016;102:843-849.

    CrossrefMedlineGoogle Scholar
  • 16. Mussatto K.A., Hoffmann R., Hoffman G., et al. "Risk factors for abnormal developmental trajectories in young children with congenital heart disease". Circulation . 2015;132:755-761.

    CrossrefMedlineGoogle Scholar
  • 17. Roberts S.D., Kazazian V., Ford M.K., et al. "The association between parent stress, coping and mental health, and neurodevelopmental outcomes of infants with congenital heart disease". Clin Neuropsychol . 2021;35:948-972.

    CrossrefMedlineGoogle Scholar
  • 18. Newburger J.W., Sleeper L.A., Bellinger D.C., et al. "Early developmental outcome in children with hypoplastic left heart syndrome and related anomalies: the single ventricle reconstruction trial". Circulation . 2012;125:2081-2091.

    CrossrefMedlineGoogle Scholar
  • 19. Jackson J.L., Leslie C.E., Hondorp S.N. "Depressive and anxiety symptoms in adult congenital heart disease: prevalence, health impact and treatment". Prog Cardiovasc Dis . 2018;61:294-299.

    CrossrefMedlineGoogle Scholar
  • 20. Khalil A., Suff N., Thilaganathan B., Hurrell A., Cooper D., Carvalho J. "Brain abnormalities and neurodevelopmental delay in congenital heart disease: systematic review and meta-analysis". Ultrasound Obstet Gynecol . 2014;43:14-24.

    CrossrefMedlineGoogle Scholar
  • 21. Lim J.M., Kingdom T., Saini B., et al. "Cerebral oxygen delivery is reduced in newborns with congenital heart disease". J Thorac Cardiovasc Surg . 2016;152:1095-1103.

    CrossrefMedlineGoogle Scholar
  • 22. Sun L., Macgowan C.K., Sled J.G., et al. "Reduced fetal cerebral oxygen consumption is associated with smaller brain size in fetuses with congenital heart disease". Circulation . 2015;131:1313-1323.

    CrossrefMedlineGoogle Scholar
  • 23. Miller S.P., McQuillen P.S., Hamrick S., et al. "Abnormal brain development in newborns with congenital heart disease". N Engl J Med . 2007;357:1928-1938.

    CrossrefMedlineGoogle Scholar
  • 24. Khalil A., Bennet S., Thilaganathan B., Paladini D., Griffiths P., Carvalho J.S. "Prevalence of prenatal brain abnormalities in fetuses with congenital heart disease: a systematic review". Ultrasound Obstet Gynecol . 2016;48:296-307.

    CrossrefMedlineGoogle Scholar
  • 25. von Rhein M., Scheer I., Loenneker T., Huber R., Knirsch W., Latal B. "Structural brain lesions in adolescents with congenital heart disease". J Pediatr . 2011;158:984-989.

    CrossrefMedlineGoogle Scholar
  • 26. Bolduc M.E., Lambert H., Ganeshamoorthy S., Brossard-Racine M. "Structural brain abnormalities in adolescents and young adults with congenital heart defect: a systematic review". Dev Med Child Neurol . 2018;60:1209-1224.

    CrossrefMedlineGoogle Scholar
  • 27. Moher D., Liberati A., Tetzlaff J., Altman D.G., PRISMA Group. "Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement". Ann Intern Med . 2009;151:264-269.

    CrossrefMedlineGoogle Scholar
  • 28. National Institutes of Health. "Study quality assessment tools. National Heart, Lung, and Blood Institute 2014". https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools. Accessed February 2, 2021.

    Google Scholar
  • 29. Andropoulos D.B., Ahmad H.B., Haq T., et al. "The association between brain injury, perioperative anesthetic exposure, and 12-month neurodevelopmental outcomes after neonatal cardiac surgery: a retrospective cohort study". Paediatr Anaesth . 2014;24:266-274.

    CrossrefMedlineGoogle Scholar
  • 30. Andropoulos D.B., Easley R.B., Brady K., et al. "Changing expectations for neurological outcomes after the neonatal arterial switch operation". Ann Thorac Surg . 2012;94:1250-1256.

    CrossrefMedlineGoogle Scholar
  • 31. Bertholdt S., Latal B., Liamlahi R., et al. "Cerebral lesions on magnetic resonance imaging correlate with preoperative neurological status in neonates undergoing cardiopulmonary bypass surgery". Eur J Cardiothorac Surg . 2014;45:625-632.

    CrossrefMedlineGoogle Scholar
  • 32. Kuhn V.A., Carpenter J.L., Zurakowski D., et al. "Determinants of neurological outcome in neonates with congenital heart disease following heart surgery". Pediatr Res . 2021;89:1283-1290.

    CrossrefMedlineGoogle Scholar
  • 33. Jakab A., Meuwly E., Feldmann M., et al. "Left temporal plane growth predicts language development in newborns with congenital heart disease". Brain . 2019;142:1270-1281.

    CrossrefMedlineGoogle Scholar
  • 34. Bellinger D.C., Jonas R.A., Rappaport L.A., et al. "Developmental and neurologic status of children after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass". N Engl J Med . 1995;332:549-555.

    CrossrefMedlineGoogle Scholar
  • 35. Cheng H.H., Wypij D., Laussen P.C., et al. "Cerebral blood flow velocity and neurodevelopmental outcome in infants undergoing surgery for congenital heart disease". Ann Thorac Surg . 2014;98:125-132.

    CrossrefMedlineGoogle Scholar
  • 36. Jenks C.L., Hernandez A., Stavinoha P.L., et al. "Elevated cranial ultrasound resistive indices are associated with improved neurodevelopmental outcomes one year after pediatric cardiac surgery: a single center pilot study". Heart Lung . 2017;46:251-257.

    CrossrefMedlineGoogle Scholar
  • 37. Ibuki K., Watanabe K., Yoshimura N., et al. "The improvement of hypoxia correlates with neuroanatomic and developmental outcomes: comparison of midterm outcomes in infants with transposition of the great arteries or single-ventricle physiology". J Thorac Cardiovasc Surg . 2012;143:1077-1085.

    CrossrefMedlineGoogle Scholar
  • 38. Mueller M., Zajonz T., Mann V., et al. "Interrelations of intraoperative changes in cerebral tissue oxygen saturation with brain volumes and neurodevelopment outcome after the comprehensive stage II procedure in infants with hypoplastic left heart syndrome: a retrospective cohort study". J Cardiothorac Vasc Anesth . 2021;35:2907-2912.

    CrossrefMedlineGoogle Scholar
  • 39. Reich B., Heye K.N., O'Gorman Tuura R., et al. "Interrelationship between hemodynamics, brain volumes, and outcome in hypoplastic left heart syndrome". Ann Thorac Surg . 2019;107:1838-1844.

    CrossrefMedlineGoogle Scholar
  • 40. Heye K.N., Knirsch W., Latal B., et al. "Reduction of brain volumes after neonatal cardiopulmonary bypass surgery in single-ventricle congenital heart disease before Fontan completion". Pediatr Res . 2018;83:63-70.

    CrossrefMedlineGoogle Scholar
  • 41. Knirsch W., Mayera K.N., Scheer I., et al. "Structural cerebral abnormalities and neurodevelopmental status in single ventricle congenital heart disease before Fontan procedure". Eur J Cardiothorac Surg . 2017;51:740-746.

    MedlineGoogle Scholar
  • 42. Lim J.M., Porayette P., Marini D., et al. "Associations between age at arterial switch operation, brain growth, and development in infants with transposition of the great arteries". Circulation . 2019;139:2728-2738.

    CrossrefMedlineGoogle Scholar
  • 43. Williams I.A., Fifer C., Jaeggi E., Levine J.C., Michelfelder E.C., Szwast A.L. "The association of fetal cerebrovascular resistance with early neurodevelopment in single ventricle congenital heart disease". Am Heart J . 2013;165:544-550.

    CrossrefMedlineGoogle Scholar
  • 44. Hahn E., Szwast A., Cnota J., et al. "Association between fetal growth, cerebral blood flow and neurodevelopmental outcome in univentricular fetuses". Ultrasound Obstet Gynecol . 2016;47:460-465.

    CrossrefMedlineGoogle Scholar
  • 45. Abeysekera J.B., Gyenes D.L., Atallah J., et al. "Fetal umbilical arterial pulsatility correlates with 2-year growth and neurodevelopmental outcomes in congenital heart disease". Can J Cardiol . 2021;37:425-432.

    CrossrefMedlineGoogle Scholar
  • 46. Gunn J.K., Beca J., Penny D.J., et al. "Amplitude-integrated electroencephalography and brain injury in infants undergoing Norwood-type operations". Ann Thorac Surg . 2012;93:170-176.

    CrossrefMedlineGoogle Scholar
  • 47. Sarajuuri A., Jokinen E., Puosi R., et al. "Neurodevelopment in children with hypoplastic left heart syndrome". J Pediatr . 2010;157:414-420.

    CrossrefMedlineGoogle Scholar
  • 48. Spaeder M.C., Klugman D., Skurow-Todd K., Glass P., Jonas R.A., Donofrio M.T. "Perioperative near-infrared spectroscopy monitoring in neonates with congenital heart disease: relationship of cerebral tissue oxygenation index variability with neurodevelopmental outcome". Pediatr Crit Care Med . 2017;18:213-218.

    CrossrefMedlineGoogle Scholar
  • 49. Toet M.C., Flinterman A., Van De Laar I., et al. "Cerebral oxygen saturation and electrical brain activity before, during, and up to 36 hours after arterial switch procedure in neonates without pre-existing brain damage: its relationship to neurodevelopmental outcome". Exp Brain Res . 2005;165:343-350.

    CrossrefMedlineGoogle Scholar
  • 50. Peyvandi S., Chau V., Guo T., et al. "Neonatal brain injury and timing of neurodevelopmental assessment in patients with congenital heart disease". J Am Coll Cardiol . 2018;71:1986-1996.

    View ArticleGoogle Scholar
  • 51. Rappaport L.A., Wypij D., Bellinger D.C., et al. "Relation of seizures after cardiac surgery in early infancy to neurodevelopmental outcome". Circulation . 1998;97:773-779.

    CrossrefMedlineGoogle Scholar
  • 52. Bellinger D.C., Wypij D., Kuban K.C.K., et al. "Developmental and neurological status of children at 4 years of age after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass". Circulation . 1999;100:526-532.

    CrossrefMedlineGoogle Scholar
  • 53. Hansen J.H., Rotermann I., Logoteta J., et al. "Neurodevelopmental outcome in hypoplastic left heart syndrome: impact of perioperative cerebral tissue oxygenation of the Norwood procedure". J Thorac Cardiovasc Surg . 2016;151:1358-1366.

    CrossrefMedlineGoogle Scholar
  • 54. Hoffman G.M., Brosig C.L., Mussatto K.A., Tweddell J.S., Ghanayem N.S. "Perioperative cerebral oxygen saturation in neonates with hypoplastic left heart syndrome and childhood neurodevelopmental outcome". J Thorac Cardiovasc Surg . 2013;146:1153-1164.

    CrossrefMedlineGoogle Scholar
  • 55. Panigrahy A., Schmithorst V.J., Wisnowski J.L., et al. "Relationship of white matter network topology and cognitive outcome in adolescents with d-transposition of the great arteries". Neuroimage Clin . 2015;7:438-448.

    CrossrefMedlineGoogle Scholar
  • 56. Rollins C.K., Watson C.G., Asaro L.A., et al. "White matter microstructure and cognition in adolescents with congenital heart disease". J Pediatr . 2014;165:936-944.

    CrossrefMedlineGoogle Scholar
  • 57. Munoz-Lopez M., Hoskote A., Chadwick M.J., et al. "Hippocampal damage and memory impairment in congenital cyanotic heart disease". Hippocampus . 2017;27:417-424.

    CrossrefMedlineGoogle Scholar
  • 58. Hiraiwa A., Kawasaki Y., Ibuki K., et al. "Brain development of children with single ventricle physiology or transposition of the great arteries: a longitudinal observation study". Semin Thorac Cardiovasc Surg . 2020;32:936-944.

    CrossrefMedlineGoogle Scholar
  • 59. Neukomm A., Ehrler M., Feldmann M., et al. "Perioperative course and socioeconomic status predict long-term neurodevelopment better than perioperative conventional neuroimaging in children with congenital heart disease". J Pediatr . 2022;251:140-148.

    CrossrefMedlineGoogle Scholar
  • 60. Heinrichs A.K.M., Holschen A., Krings T., et al. "Neurologic and psycho-intellectual outcome related to structural brain imaging in adolescents and young adults after neonatal arterial switch operation for transposition of the great arteries". J Thorac Cardiovasc Surg . 2014;148:2190-2199.

    CrossrefMedlineGoogle Scholar
  • 61. Morton S.U., Maleyeff L., Wypij D., et al. "Abnormal left-hemispheric sulcal patterns correlate with neurodevelopmental outcomes in subjects with single ventricular congenital heart disease". Cereb Cortex . 2020;30:476-487.

    CrossrefMedlineGoogle Scholar
  • 62. Watson C.G., Stopp C., Wypij D., Bellinger D.C., Newburger J.W., Rivkin M.J. "Altered white matter microstructure correlates with IQ and processing speed in children and adolescents post-Fontan". J Pediatr . 2018;200:140-149.

    CrossrefMedlineGoogle Scholar
  • 63. Calderon J., Stopp C., Wypij D., et al. "Early-term birth in single-ventricle congenital heart disease after the Fontan procedure: neurodevelopmental and psychiatric outcomes". J Pediatr . 2016;179:96-103.

    CrossrefMedlineGoogle Scholar
  • 64. Schmithorst V.J., Panigrahy A., Gaynor J.W., et al. "Organizational topology of brain and its relationship to ADHD in adolescents with d-transposition of the great arteries". Brain Behav . 2016;6:e00504.

    CrossrefMedlineGoogle Scholar
  • 65. DeMaso D.R., Labella M., Taylor G.A., et al. "Psychiatric disorders and function in adolescents with d-transposition of the great arteries". J Pediatr . 2014;165:760-766.

    CrossrefMedlineGoogle Scholar
  • 66. DeMaso D.R., Calderon J., Taylor G.A., et al. "Psychiatric disorders in adolescents with single ventricle congenital heart disease". Pediatrics . 2017;139:e20162241.

    CrossrefMedlineGoogle Scholar
  • 67. Verrall C.E., Yang J.Y.M., Chen J., et al. "Neurocognitive dysfunction and smaller brain volumes in adolescents and adults with a Fontan circulation". Circulation . 2021;143:878-891.

    CrossrefMedlineGoogle Scholar
  • 68. King T.Z., Smith K.M., Burns T.G., et al. "fMRI investigation of working memory in adolescents with surgically treated congenital heart disease". Appl Neuropsychol Child . 2017;6:7-21.

    CrossrefMedlineGoogle Scholar
  • 69. Brewster R.C., King T.Z., Burns T.G., Drossner D.M., Mahle W.T. "White matter integrity dissociates verbal memory and auditory attention span in emerging adults with congenital heart disease". J Int Neuropsychol Soc . 2015;21:22-33.

    CrossrefMedlineGoogle Scholar
  • 70. Bellinger D.C., Watson C.G., Rivkin M.J., et al. "Neuropsychological status and structural brain imaging in adolescents with single ventricle who underwent the Fontan procedure". J Am Heart Assoc . 2015;4:e002302.

    CrossrefMedlineGoogle Scholar
  • 71. Pike N.A., Roy B., Moye S., et al. "Reduced hippocampal volumes and memory deficits in adolescents with single ventricle heart disease". Brain Behav . 2021;11:e01977.

    CrossrefGoogle Scholar
  • 72. Verrall C.E., Chen J., Yeh C.-H., et al. "A diffusion MRI study of brain white matter microstructure in adolescents and adults with a Fontan circulation: investigating associations with resting and peak exercise oxygen saturations and cognition". Neuroimage Clin . 2022;36:103151.

    CrossrefMedlineGoogle Scholar
  • 73. Garfinkle J., Guo T., Synnes A., et al. "Location and size of preterm cerebellar hemorrhage and childhood development". Ann Neurol . 2020;88:1095-1108.

    CrossrefMedlineGoogle Scholar
  • 74. Ehrler M., Latal B., Kretschmar O., von Rhein M., Tuura R.O.G. "Altered frontal white matter microstructure is associated with working memory impairments in adolescents with congenital heart disease: a diffusion tensor imaging study". Neuroimage Clin . 2020;25:102123.

    CrossrefMedlineGoogle Scholar
  • 75. Ehrler M., Schlosser L., Brugger P., et al. "Altered white matter microstructure is related to cognition in adults with congenital heart disease". Brain Commun . 2021;3:fcaa224.

    CrossrefMedlineGoogle Scholar
  • 76. Ramirez A., Peyvandi S., Cox S., et al. "Neonatal brain injury influences structural connectivity and childhood functional outcomes". PloS One . 2022;17:e0262310.

    CrossrefGoogle Scholar
  • 77. Sarapas C., Shankman S.A., Harrow M., Faull R.N. "Attention/processing speed prospectively predicts social impairment 18 years later in mood disorders". J Nerv Ment Dis . 2013;201:824.

    CrossrefMedlineGoogle Scholar
  • 78. Vetter N.C., Leipold K., Kliegel M., Phillips L.H., Altgassen M. "Ongoing development of social cognition in adolescence". Child Neuropsychol . 2013;19:615-629.

    CrossrefMedlineGoogle Scholar
  • 79. Rivkin M.J., Watson C.G., Scoppettuolo L.A., et al. "Adolescents with d-transposition of the great arteries repaired in early infancy demonstrate reduced white matter microstructure associated with clinical risk factors". J Thorac Cardiovasc Surg . 2013;146:543-549.

    CrossrefMedlineGoogle Scholar
  • 80. Aly S.A., Zurakowski D., Glass P., Skurow-Todd K., Jonas R.A., Donofrio M.T. "Cerebral tissue oxygenation index and lactate at 24 hours postoperative predict survival and neurodevelopmental outcome after neonatal cardiac surgery". Congenit Heart Dis . 2017;12:188-195.

    CrossrefMedlineGoogle Scholar
  • 81. Kussman B.D., Wypij D., Laussen P.C., et al. "Relationship of intraoperative cerebral oxygen saturation to neurodevelopmental outcome and brain magnetic resonance imaging at 1 year of age in infants undergoing biventricular repair". Circulation . 2010;122:245-254.

    CrossrefMedlineGoogle Scholar
  • 82. Algra S.O., Schouten A.N., Jansen N.J., et al. "Perioperative and bedside cerebral monitoring identifies cerebral injury after surgical correction of congenital aortic arch obstruction". Intensive Care Med . 2015;41:2011-2012.

    CrossrefMedlineGoogle Scholar
  • 83. Sadhwani A., Wypij D., Rofeberg V., et al. "Fetal brain volume predicts neurodevelopment in congenital heart disease". Circulation . 2022;145:1108-1119.

    CrossrefMedlineGoogle Scholar
  • 84. Rollins C.K., Ortinau C.M., Stopp C., et al. "Regional brain growth trajectories in fetuses with congenital heart disease". Ann Neurol . 2021;89:143-157.

    CrossrefMedlineGoogle Scholar
  • 85. Schlatterer S.D., Murnick J., Jacobs M., White L., Donofrio M.T., Limperopoulos C. "Placental pathology and neuroimaging correlates in neonates with congenital heart disease". Sci Rep . 2019;9:1-11.

    CrossrefMedlineGoogle Scholar
  • 86. Homsy J., Zaidi S., Shen Y., et al. "De novo mutations in congenital heart disease with neurodevelopmental and other congenital anomalies". Science . 2015;350:1262-1266.

    CrossrefMedlineGoogle Scholar
  • 87. Kasparian N.A. "Heart care before birth: a psychobiological perspective on fetal cardiac diagnosis". Prog Pediatr Cardiol . 2019;54:101142.

    CrossrefGoogle Scholar
  • 88. Verrall C.E., Patel S., Let al Travitz "Biological and structural phenotypes associated with neurodevelopmental disability in congenital heart disease". Transl Pediatr . 2023;12:4: 768-786.

    CrossrefMedlineGoogle Scholar
  • 89. Bonthrone A.F., Chew A., Kelly C.J., et al. "Cognitive function in toddlers with congenital heart disease: the impact of a stimulating home environment". Infancy . 2021;26:184-199.

    CrossrefMedlineGoogle Scholar
  • 90. Rowlands M.A., Scheinost D., Lacadie C., et al. "Language at rest: a longitudinal study of intrinsic functional connectivity in preterm children". Neuroimage Clin . 2016;11:149-157.

    CrossrefMedlineGoogle Scholar
  • 91. Young J.M., Morgan B.R., Whyte H.E., et al. "Longitudinal study of white matter development and outcomes in children born very preterm". Cereb Cortex . 2017;27:4094-4105.

    MedlineGoogle Scholar
  • 92. Marek S., Tervo-Clemmens B., Calabro F.J., et al. "Reproducible brain-wide association studies require thousands of individuals". Nature . 2022;603:654-660.

    CrossrefMedlineGoogle Scholar
  • 93. Gray J.P., Müller V.I., Eickhoff S.B., Fox P.T. "Multimodal abnormalities of brain structure and function in major depressive disorder: a meta-analysis of neuroimaging studies". Am J Psychiatry . 2020;177:422-434.

    CrossrefMedlineGoogle Scholar
  • 94. Javaheripour N., Li M., Chand T., et al. "Altered resting-state functional connectome in major depressive disorder: a mega-analysis from the PsyMRI consortium". Transl Pychiatry . 2021;11:511.

    CrossrefMedlineGoogle Scholar
  • 95. Xu J., Van Dam N.T., Feng C., et al. "Anxious brain networks: a coordinate-based activation likelihood estimation meta-analysis of resting-state functional connectivity studies in anxiety". Neurosci Biobehav Rev . 2019;96:21-30.

    CrossrefMedlineGoogle Scholar
  • 96. Kasparian N.A., Winlaw D.S., Sholler G.F. "“Congenital heart health”: how psychological care can make a difference". Med J Aust . 2016;205:104-107.

    CrossrefMedlineGoogle Scholar
  • 97. Gee D.G., Gabard-Durnam L.J., Flannery J., et al. "Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation". Proc Natl Acad Sci U S A . 2013;110:15638-15643.

    CrossrefMedlineGoogle Scholar
  • 98. Bick J., Zhu T., Stamoulis C., Fox N.A., Zeanah C., Nelson C.A. "Effect of early institutionalization and foster care on long-term white matter development: a randomized clinical trial". JAMA Pediatr . 2015;169:211-219.

    CrossrefMedlineGoogle Scholar
  • 99. Meyer H.C., Fields A., Vanucci A., et al. "The added value of crosstalk between developmental circuit neuroscience and clinical practice to inform the treatment of adolescent anxiety". Biol Psychiatry Glob Open Sci . 2023;3:169-178.

    CrossrefMedlineGoogle Scholar
  • 100. Marino B.S., Lipkin P.H., Newburger J.W., et al. "Neurodevelopmental outcomes in children with congenital heart disease: evaluation and management: a scientific statement from the American Heart Association". Circulation . 2012;126:1143-1172.

    CrossrefMedlineGoogle Scholar