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Abstract
Magnetic resonance (MR) imaging (MRI) of the newborn brain has provided vast insight into the normal developing brain. MRI has also yielded important insights into the timing, mechanisms and the prognostic significance of neonatal brain injury. However, a number of practical limitations remain while preparing and managing the critically ill infant to safely complete optimal MR imaging. Furthermore, the interpretation of the study requires a multidisciplinary team of experienced clinicians with thorough knowledge of the unique aspects of the newborn brain. In this review, we examine the application and utility of brain MRI for preterm and term infants and those with diagnosis of perinatal stroke and congenital heart disease (CHD).
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References
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[1] Gluckman PD, Wyatt JS, Azzopardi D, Ballard R, Edwards AD, Ferriero DM, Polin RA, Robertson CM, Thoresen M, Whitelaw A, et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet. 2005 Feb 19-25;365(9460):663-70. Available from: doi: 10.1016/S0140-6736(05)17946-X.
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[3] Azzopardi DV, Strohm B, Edwards AD, Dyet L, Halliday HL, Juszczak E, Kapellou O, Levene M, Marlow N, Porter E, et al. Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med. 2009 Oct 1;361(14):1349-58. Available from: doi: 10.1056/NEJMoa0900854. Erratum in: N Engl J Med. 2010 Mar 18;362(11):1056.
[4] Jacobs SE, Berg M, Hunt R, Tarnow-Mordi WO, Inder TE, Davis PG. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev. 2013 Jan 31;2013(1):CD003311. Available from: doi: 10.1002/14651858.CD003311.pub3.
[5] Azzopardi D, Strohm B, Marlow N, Brocklehurst P, Deierl A, Eddama O, Goodwin J, Halliday HL, Juszczak E, Kapellou O, et al. Effects of hypothermia for perinatal asphyxia on childhood outcomes. N Engl J Med. 2014 Jul 10;371(2):140-9. Available from: doi: 10.1056/NEJMoa1315788.
[6] Guillet R, Edwards AD, Thoresen M, Ferriero DM, Gluckman PD, Whitelaw A, Gunn AJ; CoolCap Trial Group. Seven- to eight-year follow-up of the CoolCap trial of head cooling for neonatal encephalopathy. Pediatr Res. 2012 Feb;71(2):205-9. Available from: doi: 10.1038/pr.2011.30.
[7] Shankaran S, Pappas A, McDonald SA, Vohr BR, Hintz SR, Yolton K, Gustafson KE, Leach TM, Green C, Bara R, et al. N Engl J Med. 2012 May 31;366(22):2085-92. Available from doi: 10.1056/NEJMoa1112066. Erratum in: N Engl J Med. 2012 Sep 13;367(11):1073.
[8] Tharmapoopathy P, Chisholm P, Barlas A, Varsami M, Gupta N, Ekitzidou G, Ponnusamy V, Kappelou O, Evanson J, Rosser G, et al. In clinical practice, cerebral MRI in newborns is highly predictive of neurodevelopmental outcome after therapeutic hypothermia. Eur J Paediatr Neurol. 2020 Mar;25:127-133. Available from: doi: 10.1016/j.ejpn.2019.12.018.
[9] Lally PJ, Montaldo P, Oliveira V, Soe A, Swamy R, Bassett P, Mendoza J, Atreja G, Kariholu U, Pattnayak S, et al. Magnetic resonance spectroscopy assessment of brain injury after moderate hypothermia in neonatal encephalopathy: a prospective multicentre cohort study. Lancet Neurol. 2019 Jan;18(1):35-45. Available from: doi: 10.1016/S1474-4422(18)30325-9.
[10] Molavi M, Vann SD, de Vries LS, Groenendaal F, Lequin M. Signal Change in the Mammillary Bodies after Perinatal Asphyxia. AJNR Am J Neuroradiol. 2019 Nov;40(11):1829-1834. Available from: doi: 10.3174/ajnr.A6232.
[11] Bednarek N, Mathur A, Inder T, Wilkinson J, Neil J, Shimony J. Impact of therapeutic hypothermia on MRI diffusion changes in neonatal encephalopathy. Neurology. 2012 May 1;78(18):1420-7. Available from: doi: 10.1212/WNL.0b013e318253d589.
[12] Gano D, Chau V, Poskitt KJ, Hill A, Roland E, Brant R, Chalmers M, Miller SP. Evolution of pattern of injury and quantitative MRI on days 1 and 3 in term newborns with hypoxic-ischemic encephalopathy. Pediatr Res. 2013 Jul;74(1):82-7. Available from: doi: 10.1038/pr.2013.69.
[13] Kariholu U, Montaldo P, Markati T, Lally PJ, Pryce R, Teiserskas J, Liow N, Oliveira V, Soe A, Shankaran S, et al. Therapeutic hypothermia for mild neonatal encephalopathy: a systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed. 2020 Mar;105(2):225-228. Available from: doi: 10.1136/archdischild-2018-315711.
[14] Mikrogeorgiou A, Chen Y, Lee BS, Bok R, Sheldon RA, Barkovich AJ, Xu D, Ferriero DM. A Metabolomics Study of Hypoxia Ischemia during Mouse Brain Development Using Hyperpolarized 13C. Dev Neurosci. 2020;42(1):49-58. Available from: doi: 10.1159/000506982.
[15] Hintz SR, Barnes PD, Bulas D, Slovis TL, Finer NN, Wrage LA, Das A, Tyson JE, Stevenson DK, Carlo WA, et al. Neuroimaging and neurodevelopmental outcome in extremely preterm infants. Pediatrics. 2015 Jan;135(1):e32-42. Available from: doi: 10.1542/peds.2014-0898.
[16] Arulkumaran S, Tusor N, Chew A, Falconer S, Kennea N, Nongena P, Hajnal JV, Counsell SJ, Rutherford MA, Edwards AD. MRI Findings at Term-Corrected Age and Neurodevelopmental Outcomes in a Large Cohort of Very Preterm Infants. AJNR Am J Neuroradiol. 2020 Aug;41(8):1509-1516. Available from: doi: 10.3174/ajnr.A6666.
[17] Burkitt K, Kang O, Jyoti R, Mohamed AL, Chaudhari T. Comparison of cranial ultrasound and MRI for detecting BRAIN injury in extremely preterm infants and correlation with neurological outcomes at 1 and 3 years. Eur J Pediatr. 2019 Jul;178(7):1053-1061. Available from: doi: 10.1007/s00431-019-03388-7.
[18] Stoll BJ, Hansen NI, Bell EF, Walsh MC, Carlo WA, Shankaran S, Laptook AR, Sánchez PJ, Van Meurs KP, Wyckoff M, et al. Trends in Care Practices, Morbidity, and Mortality of Extremely Preterm Neonates, 1993-2012. JAMA. 2015 Sep 8;314(10):1039-51. Available from: doi: 10.1001/jama.2015.10244.
[19] Edwards AD, Redshaw ME, Kennea N, Rivero-Arias O, Gonzales-Cinca N, Nongena P, Ederies M, Falconer S, Chew A, Omar O, et al. Effect of MRI on preterm infants and their families: a randomised trial with nested diagnostic and economic evaluation. Arch Dis Child Fetal Neonatal Ed. 2018 Jan;103(1):F15-F21. Available from: doi: 10.1136/archdischild-2017-313102.
[20] Ibrahim J, Mir I, Chalak L. Brain imaging in preterm infants <32 weeks gestation: a clinical review and algorithm for the use of cranial ultrasound and qualitative brain MRI. Pediatr Res. 2018 Dec;84(6):799-806. Available from: doi: 10.1038/s41390-018-0194-6.
[21] Kirton A, Deveber G, Pontigon AM, Macgregor D, Shroff M. Presumed perinatal ischemic stroke: vascular classification predicts outcomes. Ann Neurol. 2008 Apr;63(4):436-43. Available from: doi: 10.1002/ana.21334.
[22] Olivé G, Agut T, Echeverría-Palacio CM, Arca G, García-Alix A. Usefulness of Cranial Ultrasound for Detecting Neonatal Middle Cerebral Artery Stroke. Ultrasound Med Biol. 2019 Mar;45(3):885-890. Available from: doi: 10.1016/j.ultrasmedbio.2018.11.004.
[23] van der Aa NE, Benders MJ, Groenendaal F, de Vries LS. Neonatal stroke: a review of the current evidence on epidemiology, pathogenesis, diagnostics and therapeutic options. Acta Paediatr. 2014 Apr;103(4):356-64. Available from: doi: 10.1111/apa.12555.
[24] Kirton A, Shroff M, Visvanathan T, deVeber G. Quantified corticospinal tract diffusion restriction predicts neonatal stroke outcome. Stroke. 2007 Mar;38(3):974-80. Available from: doi: 10.1161/01.STR.0000258101.67119.72.
[25] Wagenaar N, van der Aa NE, Groenendaal F, Verhage CH, Benders MJNL, de Vries LS. MR imaging for accurate prediction of outcome after perinatal arterial ischemic stroke: Sooner not necessarily better. Eur J Paediatr Neurol. 2017 Jul;21(4):666-670. Available from: doi: 10.1016/j.ejpn.2017.04.002.
[26] Wagenaar N, Martinez-Biarge M, van der Aa NE, van Haastert IC, Groenendaal F, Benders MJNL, Cowan FM, de Vries LS. Neurodevelopment After Perinatal Arterial Ischemic Stroke. Pediatrics. 2018 Sep;142(3):e20174164. Available from: doi: 10.1542/peds.2017-4164.
[27] Chabrier S, Peyric E, Drutel L, Deron J, Kossorotoff M, Dinomais M, Lazaro L, Lefranc J, Thébault G, Dray G, et al. Multimodal Outcome at 7 Years of Age after Neonatal Arterial Ischemic Stroke. J Pediatr. 2016 May;172:156-161.e3. Available from: doi: 10.1016/j.jpeds.2016.01.069.
[28] Larpthaveesarp A, Georgevits M, Ferriero DM, Gonzalez FF. Delayed erythropoietin therapy improves histological and behavioral outcomes after transient neonatal stroke. Neurobiol Dis. 2016 Sep;93:57-63. Available from: doi: 10.1016/j.nbd.2016.04.006.
[29] Gaynor JW, Stopp C, Wypij D, Andropoulos DB, Atallah J, Atz AM, Beca J, Donofrio MT, Duncan K, Ghanayem NS, et al. Neurodevelopmental outcomes after cardiac surgery in infancy. Pediatrics. 2015 May;135(5):816-25. Available from: doi: 10.1542/peds.2014-3825.
[30] Snookes SH, Gunn JK, Eldridge BJ, Donath SM, Hunt RW, Galea MP, Shekerdemian L. A systematic review of motor and cognitive outcomes after early surgery for congenital heart disease. Pediatrics. 2010 Apr;125(4):e818-27. Available from: doi: 10.1542/peds.2009-1959.
[31] Schaefer C, von Rhein M, Knirsch W, Huber R, Natalucci G, Caflisch J, Landolt MA, Latal B. Neurodevelopmental outcome, psychological adjustment, and quality of life in adolescents with congenital heart disease. Dev Med Child Neurol. 2013 Dec;55(12):1143-9. Available from: doi: 10.1111/dmcn.12242.
[32] Claessens NHP, Chau V, de Vries LS, Jansen NJG, Au-Young SH, Stegeman R, Blaser S, Shroff M, Haas F, Marini D, et al. Brain Injury in Infants with Critical Congenital Heart Disease: Insights from Two Clinical Cohorts with Different Practice Approaches. J Pediatr. 2019 Dec;215:75-82.e2. Available from: doi: 10.1016/j.jpeds.2019.07.017.
[33] Feldmann M, Guo T, Miller SP, Knirsch W, Kottke R, Hagmann C, Latal B, Jakab A. Delayed maturation of the structural brain connectome in neonates with congenital heart disease. Biorxiv [Preprint] 2020. Available from: doi.org/10.1101/2020.09.21.306084
[34] Miller SP, McQuillen PS, Hamrick S, Xu D, Glidden DV, Charlton N, Karl T, Azakie A, Ferriero DM, Barkovich AJ, et al. Abnormal brain development in newborns with congenital heart disease. N Engl J Med. 2007 Nov 8;357(19):1928-38. Available from: doi: 10.1056/NEJMoa067393.
[35] Guo T, Chau V, Peyvandi S, Latal B, McQuillen PS, Knirsch W, Synnes A, Feldmann M, Naef N, Chakravarty MM, et al. White matter injury in term neonates with congenital heart diseases: Topology & comparison with preterm newborns. Neuroimage. 2019 Jan 15;185:742-749. Available from: doi: 10.1016/j.neuroimage.2018.06.004.
[36] Lim JM, Porayette P, Marini D, Chau V, Au-Young SH, Saini A, Ly LG, Blaser S, Shroff M, Branson HM, et al. Associations Between Age at Arterial Switch Operation, Brain Growth, and Development in Infants With Transposition of the Great Arteries. Circulation. 2019 Jun 11;139(24):2728-2738. Available from: doi: 10.1161/CIRCULATIONAHA.118.037495.
[37] von Rhein M, Buchmann A, Hagmann C, Huber R, Klaver P, Knirsch W, Latal B. Brain volumes predict neurodevelopment in adolescents after surgery for congenital heart disease. Brain. 2014 Jan;137(Pt 1):268-76. Available from: doi: 10.1093/brain/awt322.
[38] Smyser CD, Kidokoro H, Inder TE. Magnetic resonance imaging of the brain at term equivalent age in extremely premature neonates: to scan or not to scan? J Paediatr Child Health. 2012 Sep;48(9):794-800. Available from: doi: 10.1111/j.1440-1754.2012.02535.x.
References
[2] Shankaran S, Laptook AR, Ehrenkranz RA, Tyson JE, McDonald SA, Donovan EF, Fanaroff AA, Poole WK, Wright LL, Higgins RD, et al. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med. 2005 Oct 13;353(15):1574-84. Available from: doi: 10.1056/NEJMcps050929.
[3] Azzopardi DV, Strohm B, Edwards AD, Dyet L, Halliday HL, Juszczak E, Kapellou O, Levene M, Marlow N, Porter E, et al. Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med. 2009 Oct 1;361(14):1349-58. Available from: doi: 10.1056/NEJMoa0900854. Erratum in: N Engl J Med. 2010 Mar 18;362(11):1056.
[4] Jacobs SE, Berg M, Hunt R, Tarnow-Mordi WO, Inder TE, Davis PG. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev. 2013 Jan 31;2013(1):CD003311. Available from: doi: 10.1002/14651858.CD003311.pub3.
[5] Azzopardi D, Strohm B, Marlow N, Brocklehurst P, Deierl A, Eddama O, Goodwin J, Halliday HL, Juszczak E, Kapellou O, et al. Effects of hypothermia for perinatal asphyxia on childhood outcomes. N Engl J Med. 2014 Jul 10;371(2):140-9. Available from: doi: 10.1056/NEJMoa1315788.
[6] Guillet R, Edwards AD, Thoresen M, Ferriero DM, Gluckman PD, Whitelaw A, Gunn AJ; CoolCap Trial Group. Seven- to eight-year follow-up of the CoolCap trial of head cooling for neonatal encephalopathy. Pediatr Res. 2012 Feb;71(2):205-9. Available from: doi: 10.1038/pr.2011.30.
[7] Shankaran S, Pappas A, McDonald SA, Vohr BR, Hintz SR, Yolton K, Gustafson KE, Leach TM, Green C, Bara R, et al. N Engl J Med. 2012 May 31;366(22):2085-92. Available from doi: 10.1056/NEJMoa1112066. Erratum in: N Engl J Med. 2012 Sep 13;367(11):1073.
[8] Tharmapoopathy P, Chisholm P, Barlas A, Varsami M, Gupta N, Ekitzidou G, Ponnusamy V, Kappelou O, Evanson J, Rosser G, et al. In clinical practice, cerebral MRI in newborns is highly predictive of neurodevelopmental outcome after therapeutic hypothermia. Eur J Paediatr Neurol. 2020 Mar;25:127-133. Available from: doi: 10.1016/j.ejpn.2019.12.018.
[9] Lally PJ, Montaldo P, Oliveira V, Soe A, Swamy R, Bassett P, Mendoza J, Atreja G, Kariholu U, Pattnayak S, et al. Magnetic resonance spectroscopy assessment of brain injury after moderate hypothermia in neonatal encephalopathy: a prospective multicentre cohort study. Lancet Neurol. 2019 Jan;18(1):35-45. Available from: doi: 10.1016/S1474-4422(18)30325-9.
[10] Molavi M, Vann SD, de Vries LS, Groenendaal F, Lequin M. Signal Change in the Mammillary Bodies after Perinatal Asphyxia. AJNR Am J Neuroradiol. 2019 Nov;40(11):1829-1834. Available from: doi: 10.3174/ajnr.A6232.
[11] Bednarek N, Mathur A, Inder T, Wilkinson J, Neil J, Shimony J. Impact of therapeutic hypothermia on MRI diffusion changes in neonatal encephalopathy. Neurology. 2012 May 1;78(18):1420-7. Available from: doi: 10.1212/WNL.0b013e318253d589.
[12] Gano D, Chau V, Poskitt KJ, Hill A, Roland E, Brant R, Chalmers M, Miller SP. Evolution of pattern of injury and quantitative MRI on days 1 and 3 in term newborns with hypoxic-ischemic encephalopathy. Pediatr Res. 2013 Jul;74(1):82-7. Available from: doi: 10.1038/pr.2013.69.
[13] Kariholu U, Montaldo P, Markati T, Lally PJ, Pryce R, Teiserskas J, Liow N, Oliveira V, Soe A, Shankaran S, et al. Therapeutic hypothermia for mild neonatal encephalopathy: a systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed. 2020 Mar;105(2):225-228. Available from: doi: 10.1136/archdischild-2018-315711.
[14] Mikrogeorgiou A, Chen Y, Lee BS, Bok R, Sheldon RA, Barkovich AJ, Xu D, Ferriero DM. A Metabolomics Study of Hypoxia Ischemia during Mouse Brain Development Using Hyperpolarized 13C. Dev Neurosci. 2020;42(1):49-58. Available from: doi: 10.1159/000506982.
[15] Hintz SR, Barnes PD, Bulas D, Slovis TL, Finer NN, Wrage LA, Das A, Tyson JE, Stevenson DK, Carlo WA, et al. Neuroimaging and neurodevelopmental outcome in extremely preterm infants. Pediatrics. 2015 Jan;135(1):e32-42. Available from: doi: 10.1542/peds.2014-0898.
[16] Arulkumaran S, Tusor N, Chew A, Falconer S, Kennea N, Nongena P, Hajnal JV, Counsell SJ, Rutherford MA, Edwards AD. MRI Findings at Term-Corrected Age and Neurodevelopmental Outcomes in a Large Cohort of Very Preterm Infants. AJNR Am J Neuroradiol. 2020 Aug;41(8):1509-1516. Available from: doi: 10.3174/ajnr.A6666.
[17] Burkitt K, Kang O, Jyoti R, Mohamed AL, Chaudhari T. Comparison of cranial ultrasound and MRI for detecting BRAIN injury in extremely preterm infants and correlation with neurological outcomes at 1 and 3 years. Eur J Pediatr. 2019 Jul;178(7):1053-1061. Available from: doi: 10.1007/s00431-019-03388-7.
[18] Stoll BJ, Hansen NI, Bell EF, Walsh MC, Carlo WA, Shankaran S, Laptook AR, Sánchez PJ, Van Meurs KP, Wyckoff M, et al. Trends in Care Practices, Morbidity, and Mortality of Extremely Preterm Neonates, 1993-2012. JAMA. 2015 Sep 8;314(10):1039-51. Available from: doi: 10.1001/jama.2015.10244.
[19] Edwards AD, Redshaw ME, Kennea N, Rivero-Arias O, Gonzales-Cinca N, Nongena P, Ederies M, Falconer S, Chew A, Omar O, et al. Effect of MRI on preterm infants and their families: a randomised trial with nested diagnostic and economic evaluation. Arch Dis Child Fetal Neonatal Ed. 2018 Jan;103(1):F15-F21. Available from: doi: 10.1136/archdischild-2017-313102.
[20] Ibrahim J, Mir I, Chalak L. Brain imaging in preterm infants <32 weeks gestation: a clinical review and algorithm for the use of cranial ultrasound and qualitative brain MRI. Pediatr Res. 2018 Dec;84(6):799-806. Available from: doi: 10.1038/s41390-018-0194-6.
[21] Kirton A, Deveber G, Pontigon AM, Macgregor D, Shroff M. Presumed perinatal ischemic stroke: vascular classification predicts outcomes. Ann Neurol. 2008 Apr;63(4):436-43. Available from: doi: 10.1002/ana.21334.
[22] Olivé G, Agut T, Echeverría-Palacio CM, Arca G, García-Alix A. Usefulness of Cranial Ultrasound for Detecting Neonatal Middle Cerebral Artery Stroke. Ultrasound Med Biol. 2019 Mar;45(3):885-890. Available from: doi: 10.1016/j.ultrasmedbio.2018.11.004.
[23] van der Aa NE, Benders MJ, Groenendaal F, de Vries LS. Neonatal stroke: a review of the current evidence on epidemiology, pathogenesis, diagnostics and therapeutic options. Acta Paediatr. 2014 Apr;103(4):356-64. Available from: doi: 10.1111/apa.12555.
[24] Kirton A, Shroff M, Visvanathan T, deVeber G. Quantified corticospinal tract diffusion restriction predicts neonatal stroke outcome. Stroke. 2007 Mar;38(3):974-80. Available from: doi: 10.1161/01.STR.0000258101.67119.72.
[25] Wagenaar N, van der Aa NE, Groenendaal F, Verhage CH, Benders MJNL, de Vries LS. MR imaging for accurate prediction of outcome after perinatal arterial ischemic stroke: Sooner not necessarily better. Eur J Paediatr Neurol. 2017 Jul;21(4):666-670. Available from: doi: 10.1016/j.ejpn.2017.04.002.
[26] Wagenaar N, Martinez-Biarge M, van der Aa NE, van Haastert IC, Groenendaal F, Benders MJNL, Cowan FM, de Vries LS. Neurodevelopment After Perinatal Arterial Ischemic Stroke. Pediatrics. 2018 Sep;142(3):e20174164. Available from: doi: 10.1542/peds.2017-4164.
[27] Chabrier S, Peyric E, Drutel L, Deron J, Kossorotoff M, Dinomais M, Lazaro L, Lefranc J, Thébault G, Dray G, et al. Multimodal Outcome at 7 Years of Age after Neonatal Arterial Ischemic Stroke. J Pediatr. 2016 May;172:156-161.e3. Available from: doi: 10.1016/j.jpeds.2016.01.069.
[28] Larpthaveesarp A, Georgevits M, Ferriero DM, Gonzalez FF. Delayed erythropoietin therapy improves histological and behavioral outcomes after transient neonatal stroke. Neurobiol Dis. 2016 Sep;93:57-63. Available from: doi: 10.1016/j.nbd.2016.04.006.
[29] Gaynor JW, Stopp C, Wypij D, Andropoulos DB, Atallah J, Atz AM, Beca J, Donofrio MT, Duncan K, Ghanayem NS, et al. Neurodevelopmental outcomes after cardiac surgery in infancy. Pediatrics. 2015 May;135(5):816-25. Available from: doi: 10.1542/peds.2014-3825.
[30] Snookes SH, Gunn JK, Eldridge BJ, Donath SM, Hunt RW, Galea MP, Shekerdemian L. A systematic review of motor and cognitive outcomes after early surgery for congenital heart disease. Pediatrics. 2010 Apr;125(4):e818-27. Available from: doi: 10.1542/peds.2009-1959.
[31] Schaefer C, von Rhein M, Knirsch W, Huber R, Natalucci G, Caflisch J, Landolt MA, Latal B. Neurodevelopmental outcome, psychological adjustment, and quality of life in adolescents with congenital heart disease. Dev Med Child Neurol. 2013 Dec;55(12):1143-9. Available from: doi: 10.1111/dmcn.12242.
[32] Claessens NHP, Chau V, de Vries LS, Jansen NJG, Au-Young SH, Stegeman R, Blaser S, Shroff M, Haas F, Marini D, et al. Brain Injury in Infants with Critical Congenital Heart Disease: Insights from Two Clinical Cohorts with Different Practice Approaches. J Pediatr. 2019 Dec;215:75-82.e2. Available from: doi: 10.1016/j.jpeds.2019.07.017.
[33] Feldmann M, Guo T, Miller SP, Knirsch W, Kottke R, Hagmann C, Latal B, Jakab A. Delayed maturation of the structural brain connectome in neonates with congenital heart disease. Biorxiv [Preprint] 2020. Available from: doi.org/10.1101/2020.09.21.306084
[34] Miller SP, McQuillen PS, Hamrick S, Xu D, Glidden DV, Charlton N, Karl T, Azakie A, Ferriero DM, Barkovich AJ, et al. Abnormal brain development in newborns with congenital heart disease. N Engl J Med. 2007 Nov 8;357(19):1928-38. Available from: doi: 10.1056/NEJMoa067393.
[35] Guo T, Chau V, Peyvandi S, Latal B, McQuillen PS, Knirsch W, Synnes A, Feldmann M, Naef N, Chakravarty MM, et al. White matter injury in term neonates with congenital heart diseases: Topology & comparison with preterm newborns. Neuroimage. 2019 Jan 15;185:742-749. Available from: doi: 10.1016/j.neuroimage.2018.06.004.
[36] Lim JM, Porayette P, Marini D, Chau V, Au-Young SH, Saini A, Ly LG, Blaser S, Shroff M, Branson HM, et al. Associations Between Age at Arterial Switch Operation, Brain Growth, and Development in Infants With Transposition of the Great Arteries. Circulation. 2019 Jun 11;139(24):2728-2738. Available from: doi: 10.1161/CIRCULATIONAHA.118.037495.
[37] von Rhein M, Buchmann A, Hagmann C, Huber R, Klaver P, Knirsch W, Latal B. Brain volumes predict neurodevelopment in adolescents after surgery for congenital heart disease. Brain. 2014 Jan;137(Pt 1):268-76. Available from: doi: 10.1093/brain/awt322.
[38] Smyser CD, Kidokoro H, Inder TE. Magnetic resonance imaging of the brain at term equivalent age in extremely premature neonates: to scan or not to scan? J Paediatr Child Health. 2012 Sep;48(9):794-800. Available from: doi: 10.1111/j.1440-1754.2012.02535.x.