Register      Login

VOLUME 3 , ISSUE 2 ( April-June, 2024 ) > List of Articles


Utility of Point-of-care Ultrasound in Hypoxic-ischemic Brain Injury in Neonates

Gunjana Kumar, Sujata Deshpande, Sreevidya Sreekantha, Alex Stevenson, Anu Sharma, Jayanta Hazarika, Poonam Agrawal, Kirti Naranje, Akhil Maheshwari, Pradeep Suryawanshi

Keywords : Basal ganglia, Birth asphyxia, Cerebral Doppler, Cranial ultrasound, Echogenicity, Four-column sign, Hypoxic-ischemic encephalopathy, Neonates, Periventricular leukomalacia, PLIC sign

Citation Information : Kumar G, Deshpande S, Sreekantha S, Stevenson A, Sharma A, Hazarika J, Agrawal P, Naranje K, Maheshwari A, Suryawanshi P. Utility of Point-of-care Ultrasound in Hypoxic-ischemic Brain Injury in Neonates. 2024; 3 (2):124-138.

DOI: 10.5005/jp-journals-11002-0091

License: CC BY-NC 4.0

Published Online: 21-06-2024

Copyright Statement:  Copyright © 2024; The Author(s).


Background: Perinatal asphyxia and resulting hypoxic-ischemic encephalopathy (HIE) remain a significant cause of neonatal morbidity and mortality. This review focuses on the utilization of bedside cranial ultrasound in HIE to guide appropriate therapy, monitor disease progress, provide prognostic information, and help identify relevant research areas. Methods: A comprehensive literature search was conducted to review recognized patterns of HIE seen on ultrasound. Further efforts were focused on understanding the clinical relevance of these changes in the management of such infants and the prediction of long-term neurodevelopmental outcomes. Results: We reviewed cranial sonographic changes in asphyxiated neonates. Dynamic changes are observed across various time frames; hyperechogenicity of the thalamus, basal ganglia, and the altered appearance of the posterior limb of the internal capsule (PLIC) are frequently seen in acute and subacute insults. Also, a resistive index of 0.55 or less in cerebral Doppler studies within the first 72 hours of life is associated with adverse short- and long-term outcomes and increased mortality. Conclusion: Bedside cranial ultrasound is a useful screening tool for the diagnosis and monitoring of neonates with HIE. However, further studies are needed to improve our understanding of sonographic findings as predictors of adverse neurodevelopmental outcomes and mortality in affected neonates.

PDF Share
  1. Odd D, Heep A, Luyt K, et al. Hypoxic-ischemic brain injury: Planned delivery before intrapartum events. J Neonatal Perinatal Med 2017;10(4):347–353. DOI: 10.3233/NPM-16152.
  2. Desalew A, Semahgn A, Tesfaye G. Determinants of birth asphyxia among newborns in Ethiopia: A systematic review and meta-analysis. Int J Health Sci 2020;14(1):35. PMID: 32082102.
  3. Cizmeci MN, Wilson D, Singhal M, et al. Neonatal hypoxic-ischemic encephalopathy spectrum: Severity-stratified analysis of neuroimaging modalities and association with neurodevelopmental outcomes. J Pediatr 2024;266:113866. DOI:10.1016/j.jpeds.2023.113866.
  4. van Kooij BJ, van Handel M, Nievelstein RA, et al. Serial MRI and neurodevelopmental outcome in 9-to 10-year-old children with neonatal encephalopathy. J Pediatr 2010;157(2):221–227. DOI:10.1016/j.jpeds.2010.02.016.
  5. Stewart DL, Elsayed Y, Fraga MV, et al. Use of point-of-care ultrasonography in the NICU for diagnostic and procedural purposes. Pediatrics 2022;150(6):e2022060053. DOI: 10.1542/peds.2022-060053.
  6. Epelman M, Daneman A, Kellenberger CJ, et al. Neonatal encephalopathy: A prospective comparison of head US and MRI. Pediatr Radiol 2010;40(10):1640–1650. DOI: 10.1007/s00247-010-1634-6.
  7. Dzikiene R, Lukosevicius S, Laurynaitiene J, et al. The value of ultrasonography in predicting outcomes at an early school age among individuals with perinatal hypoxic-ischemic encephalopathy. Signa Vitae 2022;18(4):81–90. DOI: 10.22514/sv.2022.010.
  8. Leijser LM, De Vries LS, Rutherford MA, et al. Cranial ultrasound in metabolic disorders presenting in the neonatal period: Characteristic features and comparison with MR imaging. Am J Neuroradiol 2007;28(7):1223–1231. DOI: 10.3174/ajnr.A0553.
  9. de Vries LS, Steggerda SJ, Groenendaal F, et al. Comment on ‘value of cranial ultrasound at initiation of therapeutic hypothermia for neonatal encephalopathy’. J Perinatol 2022;42(3):418–419. DOI: 10.1038/s41372-021-01307-z.
  10. Sanislow W, Singh E, Yang E, et al. Value of cranial ultrasound at initiation of therapeutic hypothermia for neonatal encephalopathy. J Perinatol 2022;42(3):335–340. DOI: 10.1038/s41372-021-01233-0.
  11. Steggerda SJ, Leijser LM, Walther FJ, et al. Neonatal cranial ultrasonography: How to optimize its performance. Early Hum Dev 2009;85(2):93–99. DOI: 10.1016/j.earlhumdev.2008.11.008.
  12. Rath C, Suryawanshi P. Point of care neonatal ultrasound—head, lung, gut and line localization. Indian Pediatr 2016;53(10):889–899. DOI: 10.1007/s13312-016-0954-5.
  13. Daneman A, Epelman M, Blaser S, et al. Imaging of the brain in full-term neonates: Does sonography still play a role? Pediatr Radiol 2006;36(7):636–646. DOI: 10.1007/s00247-006-0201-7.
  14. Yikilmaz A, Taylor GA. Cranial sonography in term and near-term infants. Pediatr Radiol 2008;38(6)605–616. DOI:10.1007/s00247-007-0692-x.
  15. Gunn AJ, Laptook AR, Robertson NJ, et al. Therapeutic hypothermia translates from ancient history in to practice. Pediatr Res 2017;81(1):202–209. DOI: 10.1038/pr.2016.198.
  16. Ferriero DM. Neonatal brain injury. N Engl J Med 2004;351(19): 1985–1995. DOI: 10.1056/NEJMra041996.
  17. Salas J, Tekes A, Hwang M, et al. Head ultrasound in neonatal hypoxic-ischemic injury and its mimickers for clinicians: A review of the patterns of injury and the evolution of findings over time. Neonatology 2018;114(3):185–197. DOI: 10.1159/000487913.
  18. Annink KV, de Vries LS, Groenendaal F, et al. The development and validation of a cerebral ultrasound scoring system for infants with hypoxic-ischaemic encephalopathy. Pediatr Res 2020;87(Suppl 1): 59–66. DOI: 10.1038/s41390-020-0782-0.
  19. Pinto PS, Tekes A, Singhi S, et al. White–gray matter echogenicity ratio and resistive index: Sonographic bedside markers of cerebral hypoxic–ischemic injury/edema? J Perinatol 2012;32(6):448–453. DOI: 10.1038/jp.2011.121.
  20. Nelson MD, Tavaré CJ, Petrus L, et al. Changes in the size of the lateral ventricles in the normal-term newborn following vaginal delivery. Pediatr Radiol 2003;33(12):831–835. DOI: 10.1007/s00247-003-0967-9.
  21. Hwang M. Gray-scale ultrasound findings of hypoxic-ischemic injury in term infants. Pediatr Radiol 2021;51(9):1738–1747. DOI: 10.1007/s00247-021-04983-3.
  22. Wisnowski JL, Wintermark P, Bonifacio SL, et al. Neuroimaging in the term newborn with neonatal encephalopathy. Semin Fetal Neonatal Med 2021;26(5):101304. DOI: 10.1016/j.siny.2021.101304.
  23. Myers RE. Four patterns of perinatal brain damage and their conditions of occurrence in primates. Adv Neurol 1975;10:223–234. PMID: 238372.
  24. Azzarelli B, Caldemeyer KS, Phillips JP, et al. Hypoxic-ischemic encephalopathy in areas of primary myelination: a neuroimaging and PET study. Pediatr Neurol 1996;14(2):108–116. DOI: 10.1016/0887-8994(96)00010-0.
  25. Johnston MV, Hoon Jr AH. Possible mechanisms in infants for selective basal ganglia damage from asphyxia, kernicterus, or mitochondrial encephalopathies. J Child Neurol 2000;15(9):588–591. DOI: 10.1177/088307380001500904.
  26. Swarte R, Lequin M, Cherian P, et al. Imaging patterns of brain injury in term-birth asphyxia. Acta Paediatr 2009;98(3):586–592. DOI: 10.1111/j.1651-2227.2008.01156.x.
  27. Rutherford MA, Pennock JM, Dubowitz LM. Cranial ultrasound and magnetic resonance imaging in hypoxic-ischaemic encephalopathy: A comparison with outcome. Develop Med Child Neurol 1994;36(9):813–825. DOI: 10.1111/j.1469-8749.1994.tb08191.x.
  28. Martinez-Biarge M, Diez-Sebastian J, Kapellou O, et al. Predicting motor outcome and death in term hypoxic-ischemic encephalopathy. Neurology 2011;76(24):2055–2061. DOI: 10.1212/WNL.0b013e31821f442d.
  29. Pasternak JF, Gorey MT. The syndrome of acute near-total intrauterine asphyxia in the term infant. Pediatr Neurol 1998;18(5):391–398. DOI: 10.1016/S0887-8994(98)00002-2.
  30. Volpe JJ, Herscovitch P, Perlman JM, et al. Positron emission tomography in the asphyxiated term newborn: Parasagittal impairment of cerebral blood flow. Ann Neurol1985;17(3):287–296. DOI:10.1002/ana.410170312.
  31. Chacko A, Andronikou S, Mian A, et al. Cortical ischaemic patterns in term partial-prolonged hypoxic-ischaemic injury—the inter-arterial watershed demonstrated through atrophy, ulegyria and signal change on delayed MRI scans in children with cerebral palsy. Insights Imaging 2020;11(1):1–3. DOI: 10.1186/s13244-020-00857-8.
  32. Miller SP, Ramaswamy V, Michelson D, et al. Patterns of brain injury in term neonatal encephalopathy. J Pediatr 2005;146(4):453–460. DOI: 10.1016/j.jpeds.2004.12.026.
  33. Okereafor A, Allsop J, Counsell SJ, et al. Patterns of brain injury in neonates exposed to perinatal sentinel events. Pediatrics 2008;121(5):906–914. DOI: 10.1542/peds.2007-0770.
  34. Basiri B, Sabzehei M. Predictive factors of death in neonates with hypoxic-ischemic encephalopathy receiving selective head cooling. Clin Exper Pediatr 2021;64(4):180. DOI: 10.3345/cep.2019. 01382.
  35. Bano S, Chaudhary V, Garga UC. Neonatal hypoxic-ischemic encephalopathy: A radiological review. Journal of Pediatr Neurosci 2017;12(1):1. DOI: 10.4103%2F1817-1745.205646.
  36. Connolly DJ, Widjaja E, Griffiths PD. Involvement of the anterior lobe of the cerebellar vermis in perinatal profound hypoxia. Am J Neuroradiol 2007;28(1):16–19. PMID: 17213415.
  37. Hwang M, Tierradentro-García LO, Hussaini SH, et al. Ultrasound imaging of preterm brain injury: Fundamentals and updates. Pediatr Radiol 2022;52(4):817–836. DOI: 10.1007/s00247-021-05191-9.
  38. Herma P, Kalola J, Sood M, et al. Transcranial ultrasound: Efficient screening tool for detection of hypoxic brain injury in neonates–study of 50 patients. Int J Contemp Med Surg Radiol 2018;3(3):93–95. DOI: 10.21276/ijcmsr.2018.3.3.20.
  39. Liu L. Application of brain ultrasound in premature infants with brain injury. Front Neurol 2023;14:1095280. DOI: 10.3389/fneur.2023.1095280.
  40. van Wezel-Meijler G, Leijser LM, Wiggers-de Bruïne FT, et al. Diffuse hyperechogenicity of basal ganglia and thalami in preterm neonates: A physiologic finding? Radiology 2011;258(3):944–950. DOI: 10.1148/radiol.10101086.
  41. Cheong JL, Coleman L, Hunt RW, et al. Prognostic utility of magnetic resonance imaging in neonatal hypoxic-ischemic encephalopathy: Substudy of a randomized trial. Arch Pediatr Adolesc Med 2012;166(7):634–640. DOI: 10.1001/archpediatrics.2012.284.
  42. Azzopardi D, Brocklehurst P, Edwards D, et al. The TOBY Study. Whole body hypothermia for the treatment of perinatal asphyxial encephalopathy: A randomised controlled trial. BMC Pediatr 2008;8:1–2. DOI: 10.1186/1471-2431-8-17.
  43. Bednarek N, Mathur A, Inder T, et al. Impact of therapeutic hypothermia on MRI diffusion changes in neonatal encephalopathy. Neurology 2012;78(18):1420–1427. DOI: 10.1212/WNL.0b013e318253d589.
  44. Wang J, Li J, Yin X, et al. Cerebral hemodynamics of hypoxic-ischemic encephalopathy neonates at different ages detected by arterial spin labeling imaging. Clin Hemorheol Microcirc 2022;81(4):271–279. DOI: 10.3233/CH-211324.
  45. Wintermark P, Hansen A, Gregas MC, et al. Brain perfusion in asphyxiated newborns treated with therapeutic hypothermia. Am J Neuroradiol 2011;32(11):2023–2029. DOI: 10.3174/ajnr.A2708.
  46. van Bel F, Dorrepaal CA, Benders MJ, et al. Changes in cerebral hemodynamics and oxygenation in the first 24 hours after birth asphyxia. Pediatrics 1993;92(3):365–372. DOI: 10.1542/peds.92. 3.365.
  47. Perlman JM. Summary proceedings from the neurology group on hypoxic-ischemic encephalopathy. Pediatrics 2006;117(Supplement_1):S28–S33. DOI: 10.1542/peds.2005-0620E.
  48. Greisen G. Autoregulation of cerebral blood flow in newborn babies. Early Hum Dev 2005;81(5):423–428. DOI:10.1016/j.earlhumdev.2005.03.005.
  49. Volpe JJ, Inder TE, Darras BT, et al., editors. Copyright. In: Volpe's Neurology of the Newborn (Sixth Edition) [Internet]. Amsterdam, USA: Elsevier; 2018 [cited 2024 Jan 8]. p. iv. Available from:
  50. Orman G, Benson JE, Kweldam CF, et al. Neonatal head ultrasonography today: A powerful imaging tool! J Neuroimaging 2015;25(1):31–55. DOI: 10.1111/jon.12108.
  51. Pang R, Mintoft A, Crowley R, et al. Optimizing hemodynamic care in neonatal encephalopathy. Semin Fetal Neonatal Med 2020;25(5):101139 DOI: 10.1016/j.siny.2020.101139.
  52. Laptook AR, Corbett RJ. The effects of temperature on hypoxic-ischemic brain injury. Clinics in Perinatology. 2002;29(4):623–649. DOI: 10.1016/S0095-5108(02)00057-X.
  53. Skranes JH, Elstad M, Thoresen M, et al. Hypothermia makes cerebral resistance index a poor prognostic tool in encephalopathic newborns. Neonatology 2014;106(1):17–23. DOI: 10.1159/000358229.
  54. Ilves P, Lintrop M, Metsvaht T, et al. Cerebral blood-flow velocities in predicting outcome of asphyxiated newborn infants. Acta Paediatr 2004;93(4):523–528. DOI: 10.1080/08035250410024745.
  55. Liu JX, Fang CL, Zhang K, et al. Transcranial doppler ultrasonography detection on cerebrovascular flow for evaluating neonatal hypoxic-ischemic encephalopathy modeling. Front Neurosci 2023;17:962001. DOI:10.3389/fnins.2023.962001.
  56. Kirimi E, Tuncer O, Atas B, et al. Clinical value of color Doppler ultrasonography measurements of full-term newborns with perinatal asphyxia and hypoxic ischemic encephalopathy in the first 12 hours of life and long-term prognosis. Tohoku J Exper Med 2002;197(1):27–33. DOI:10.1620/tjem.197.27.
  57. Archer LN, Levene MI, Evans DH. Cerebral artery Doppler ultrasonography for prediction of outcome after perinatal asphyxia. Lancet 1986;328(8516):1116–1118. DOI: 10.1016/S0140-6736(86) 90528-3.
  58. Stark JE, Seibert JJ. Cerebral artery Doppler ultrasonography for prediction of outcome after perinatal asphyxia. J Ultrasound Med 1994;13(8):595–600. DOI: 10.7863/jum.1994.13.8.595.
  59. Elstad M, Whitelaw A, Thoresen M. Cerebral Resistance Index is less predictive in hypothermic encephalopathic newborns. Acta Paediatr 2011;100(10):1344–1349. DOI: 10.1111/j.1651-2227.2011.02327.x.
  60. Liu Y, Harder DR, Lombard JH. Interaction of myogenic mechanisms and hypoxic dilation in rat middle cerebral arteries. Am J Physiol Heart Circ Physiol 2002;283(6):H2276–H2281. DOI: 10.1152/ajpheart.00635.2002.
  61. Haaland K, Karlsson B, Skovlund E, et al. Simultaneous measurements of cerebral circulation with electromagnetic flowmetry and Doppler ultrasound velocity in the newborn pig. Pediatric Res 1994;36(5): 601–606. DOI:10.1203/00006450-199411000-00011.
  62. Liu J, Cao HY, Huang XH, et al. The pattern and early diagnostic value of Doppler ultrasound for neonatal hypoxic-ischemic encephalopathy. J Tropical Pediatrics 2007;53(5):351–354. DOI:10.1093/tropej/fmm046.
  63. Rath C, Rao S, Suryawanshi P, et al. Does abnormal Doppler on cranial ultrasound predict disability in infants with hypoxic-ischaemic encephalopathy? A systematic review. Develop Med Child Neurol 2022;64(10):1202–1213. DOI: 10.1111/dmcn.15236.
  64. Liu W, Yang Q, et al. Prognostic value of clinical tests in neonates with hypoxic-ischemic encephalopathy treated with therapeutic hypothermia: A systematic review and meta-analysis. Front Neurol 2020;25;11:133. DOI: 10.3389/fneur.2020.00133.
  65. Tann CJ, Nakakeeto M, Hagmann C, et al. Early cranial ultrasound findings among infants with neonatal encephalopathy in Uganda: An observational study. Pediatr Res 2016;80(2):190–196. DOI: 10.1038/pr.2016.77.
  66. Clay DE, Linke AC, Cameron DJ, et al. Evaluating affordable cranial ultrasonography in East African neonatal intensive care units. Ultrasound Med Biol 2017;43(1):119–128. DOI: 10.1016/j.ultrasmedbio.2016.07.024.
  67. Eken P, Jansen GH, Groenendaal F, et al. Intracranial lesions in the full-term infant with hypoxic ischaemic encephalopathy: Ultrasound and autopsy correlation. Neuropediatrics 1994;25(06):301–307. DOI: 10.1055/s-2008-1073044.
  68. Leijser LM, Vein AA, Liauw L, et al. Prediction of short-term neurological outcome in full-term neonates with hypoxic-ischaemic encephalopathy based on combined use of electroencephalogram and neuro-imaging. Neuropediatrics 2007;38(05):219–227. DOI: 10.1055/s-2007-992815.
  69. Adami RR, Grundy ME, Poretti A, et al. Distinguishing arterial ischemic stroke from hypoxic–ischemic encephalopathy in the neonate at birth. Obstetr Gynecol 2016;128(4):704. DOI:10.1097% 2FAOG.0000000000001631.
  70. Luo L, Chen D, Qu Y, et al. Association between hypoxia and perinatal arterial ischemic stroke: A meta-analysis. PLoS One 2014;9(2):e90106. DOI: 10.1371/journal.pone.0090106.
  71. Martinez-Biarge M, Cheong JL, Diez-Sebastian J, et al. Risk factors for neonatal arterial ischemic stroke: The importance of the intrapartum period. J Pediatr 2016;173:62–68. DOI: 10.1016/j.jpeds.2016.02.064.
  72. Radicioni M, Bini V, Chiarini P, et al. Cerebral sinovenous thrombosis in the asphyxiated cooled infants: A prospective observational study. Pediatric Neurol 2017;66:63–68. DOI: 10.1016/j.pediatrneurol.2016.09.006.
  73. Al Yazidi G, Boudes E, Tan X, et al. Intraventricular hemorrhage in asphyxiated newborns treated with hypothermia: A look into incidence, timing and risk factors. BMC Pediatr 2015;15(1):1–9. DOI: 10.1186/s12887-015-0415-7.
  74. Malarbi S, Gunn-Charlton JK, Burnett AC, et al. Outcome of vein of Galen malformation presenting in the neonatal period. Arch Dis Child 2019;104(11):1064–1069. DOI: 10.1136/archdischild-2018-316495.
  75. Delaney HM, Rooks VJ, Wolfe SQ, et al. Term neonate with intracranial hemorrhage and hereditary hemorrhagic telangiectasia: A case report and review of the literature. J Perinatol 2012;32(8):642–644. DOI: 10.1038/jp.2011.146.
  76. Giorgi L, Durand P, Morin L, et al. Management and outcomes of neonatal arteriovenous brain malformations with cardiac failure: A 17 Years’ experience in a tertiary referral center. J Pediatr 2020;218:85–91. DOI: 10.1016/j.jpeds.2019.10.090.
  77. Ejike O, Odume C, Ekwochi U, et al. A rare type of congenital Sturge-Weber Syndrome: Presenting with history of perinatal asphyxia. Clin Case Rep 2016;4(8):725. DOI: 10.1002/ccr3.561.
  78. El-Dib M, Parziale MP, Johnson L, et al. Encephalopathy in neonates with subgaleal hemorrhage is a key predictor of outcome. Pediatr Res 2019;86(2):234–241. DOI: 10.1038/s41390-019-0400-1.
  79. Colditz MJ, Lai MM, Cartwright DW, et al. Subgaleal haemorrhage in the newborn: A call for early diagnosis and aggressive management. J Paediatr Child Health 2015;51(2):140–146. DOI: 10.1111/jpc.12698.
  80. Teixeira J, Zimmerman R, Haselgrove J, et al. Diffusion imaging in pediatric central nervous system infections. Neuroradiology 2001;43(12):1031–1039. DOI: 10.1007/s002340100625.
  81. Mallard C, Wang X. Infection-induced vulnerability of perinatal brain injury. Neurol Res Int 2012;2012:102153. DOI: 10.1155/2012/102153.
  82. Nelson KB, Leviton A. How much of neonatal encephalopathy is due to birth asphyxia? Am J Dis Child 1991;145(11):1325–1331. DOI: 10.1001/archpedi.1991.02160110117034.
  83. Aslam S, Strickland T, Molloy EJ. Neonatal encephalopathy: Need for recognition of multiple etiologies for optimal management. Front Pediatr 2019;7:142. DOI: 10.3389/fped.2019.00142.
  84. Martinello KA, Meehan C, Avdic-Belltheus A, et al. Acute LPS sensitization and continuous infusion exacerbates hypoxic brain injury in a piglet model of neonatal encephalopathy. Sci Rep 2019;9(1):10184. DOI: 10.1038/s41598-019-46488-y.
  85. Weeke LC, Brilstra E, Braun KP, et al. Punctate white matter lesions in full-term infants with neonatal seizures associated with SLC13A5 mutations. Eur J Paediatr Neurol 2017;21(2):396–403. DOI: 10.1016/j.ejpn.2016.11.002.
  86. Executive Summary: Neonatal Encephalopathy and Neurologic Outcome, Second Edition. Obstetr Gynecol 2014;123(4):896–901. DOI: 10.1097/01.AOG.0000445580.65983.d2.
  87. Glass HC. Hypoxic-ischemic encephalopathy and other neonatal encephalopathies. Continuum (Minneap Minn) 2018;24(1):57–71. DOI: 10.1212/CON.0000000000000557.
  88. Fay AJ. Neuromuscular diseases of the newborn. Semin Pediatr Neurol 2019;32:100771. Doi: 10.1016/j.spen.2019.08.007.
  89. Durbeej M. Laminin-α2 chain-deficient congenital muscular dystrophy: Pathophysiology and development of treatment. Curr Top Membr 2015;76:31–60. DOI: 10.1016/bs.ctm.2015.05.002.
  90. Dowling JJ, Gonorazky HD, Cohn RD, et al. Treating pediatric neuromuscular disorders: The future is now. Am J Med Genet Part A 2018;176(4):804–841. DOI: 10.1002/ajmg.a.38418.
  91. Gonçalves FG, Tomás de Andrade LF, Taranath A, et al. Tubulinopathies. Top Magn Reson Imaging 2018;27(6):395–408. DOI: 10.1097/RMR.0000000000000188.
  92. Bahi-Buisson N, Poirier K, Fourniol F, et al. The wide spectrum of tubulinopathies: What are the key features for the diagnosis? Brain 2014;137(6):1676–1700. DOI: 10.1093/brain/awu082.
  93. Bahi-Buisson N, Guerrini R. Diffuse malformations of cortical development. Handbook Clin Neurol 2013;111:653–665. DOI: 10.1016/B978-0-444-52891-9.00068-3.
  94. Hahn JS, Barnes PD. Neuroimaging advances in holoprosencephaly: Refining the spectrum of the midline malformation. Am J Med Genet Part C Semin Med Genet 2010154(1):120–132. DOI10.1002/ajmg.c.30238.
  95. Brancati F, Dallapiccola B, Valente EM. Joubert Syndrome and related disorders. Orphanet J Rare Dis 2010;5:1–20. DOI: 10.1186/1750-1172-5-20.
  96. Gleeson JG, Keeler LC, Parisi MA, et al. Molar tooth sign of the midbrain–hindbrain junction: Occurrence in multiple distinct syndromes. Am J Med GenetA 2004;125(2):125–134. Doi:10.1002/ajmg.a.20437.
  97. Cormand B, Pihko H, Bayes M, et al. Clinical and genetic distinction between Walker–Warburg syndrome and muscle–eye–brain disease. Neurology 2001;56(8):1059–1069. DOI: 10.1212/WNL.56.8.1059.
  98. Hirsch JF, Pierre-Kahn A, Renier D, et al. The Dandy-Walker malformation: A review of 40 cases. J Neurosurg 1984;61(3):515–522. DOI: 10.3171/jns.1984.61.3.0515.
  99. Westerlinck H, Meylaerts L, Van Hoestenberghe MR, et al. Sulfite oxidase deficiency in a newborn. J Belg Soc Radiol 2014;97(2):113–114. DOI: 10.5334/jbr-btr.40.
  100. Chen LW, Tsai YS, Huang CC. Prenatal multicystic encephalopathy in isolated sulfite oxidase deficiency with a novel mutaion. Pediatr Neurol 2014;51(1):181–182. DOI: 10.1016/j.pediatrneurol.2014. 03.010.
  101. Hoffmann C, Ben-Zeev B, Anikster Y, et al. Magnetic resonance imaging and magnetic resonance spectroscopy in isolated sulfite oxidase deficiency. J Child Neurol 2007;22(10):1214–1221. DOI: 10.1177/0883073807306260.
  102. Serrano M, Lizarraga I, Reiss J, et al. Cranial ultrasound and chronological changes in molybdenum cofactor deficiency. Pediatr Radiol 2007;37(10):1043–1046. DOI: 10.1007/s00247-007-0558-2.
  103. Luisiri A, Sotelo-Avila C, Silberstein MJ, et al. Sonography of the Zellweger syndrome. J Ultrasound Med 1988;7(3):169–173. DOI: 10.7863/jum.1988.7.3.169.
  104. Mochel F, Grébille AG, Benachi A, et al. Contribution of fetal MR imaging in the prenatal diagnosis of Zellweger syndrome. Am J Neuroradiol 2006;27(2):333–336. PMID: 16484405.
  105. Paupe A, Bidat L, Sonigo P, et al. Prenatal diagnosis of hypoplasia of the corpus callosum in association with non-ketotic hyperglycinemia. Ultrasound Obstetr Gynecol 2002;20(6):616–619. DOI: 10.1046/j.1469-0705.2002.00869.x.
  106. McAdams RM, Richards TL. Detection of nonketotic hyperglycinemia in a neonate using proton magnetic resonance spectroscopy. Radiol Case Rep 2009;4(4):310. DOI: 10.2484/rcr.v4i4.310.
  107. Fariello G, Dionisi-Vici C, Orazi C, et al. Cranial ultrasonography in maple syrup urine disease. Am J Neuroradiol 1996;17(2):311–315. PMID: 8938303.
  108. Benson JE, Bishop MR, Cohen HL. Intracranial neonatal neurosonography: An update. Ultrasound Quarterly 2002;18(2): 89–114. DOI: 10.1097/00013644-200206000-00003.
  109. Eken P, Toet MC, Groenendaal F, et al. Predictive value of early neuroimaging, pulsed Doppler and neurophysiology in full term infants with hypoxic-ischaemic encephalopathy. Arch Dis Child 1995;73(2):F75. DOI: 10.1136/fn.73.2.f75.
  110. Cassia GS, Faingold R, Bernard C, et al. Neonatal hypoxic-ischemic injury: Sonography and dynamic color Doppler sonography perfusion of the brain and abdomen with pathologic correlation. Am J Roentgenol 2012;199(6):W743–W752. DOI: 10.2214/AJR.11. 8072.
  111. Mahantesh SK, Das SK, Patil V, et al. Predictive accuracy of duplex sonography vs. MRI in grading of neonatal hypoxic encephalopathy. 2020;3(1):01-04. DOI: 10.33545/26644436.2020.v3.i1a.49.
  112. Aun AE, Hassan HA, Ali WI, et al. Transcranial ultrasound in comparison to MRI in evaluation of hypoxic ischemic injury in neonates. Egypt J Hosp Med 2019;74(4):842–852. DOI: 10.21608/ejhm.2019.25263.
  113. Merchant N, Azzopardi D. Early predictors of outcome in infants treated with hypothermia for hypoxic–ischaemic encephalopathy. Dev Med Child Neurol 2015;57:8–16. DOI: 10.1111/dmcn.12726.
  114. Van Cauter S, Severino M, Ammendola R, et al. Bilateral lesions of the basal ganglia and thalami (central grey matter)—pictorial review. Neuroradiology 2020;62(12):1565–1605. DOI: 10.1007/s00234-020-02511-y.
  115. Sinclair DB, Campbell M, Byrne P, et al. EEG and long-term outcome of term infants with neonatal hypoxic-ischemic encephalopathy. Clin Neurophysiol 1999;110(4):655–659. DOI: 10.1016/S1388-2457(99)00010-3.
  116. Guan B, Dai C, Zhang Y, et al. Early diagnosis and outcome prediction of neonatal hypoxic-ischemic encephalopathy with color Doppler ultrasound. Diagn Interv Imaging 2017;98(6):469–475. DOI: 10.1016/j.diii.2016.12.001.
  117. Robertson C, Finer N. Term infants with hypoxic-ischemic encephalopathy: Outcome at 3.5 years. Dev Med Child Neurol 1985;27(4):473–484. DOI: 10.1111/j.1469-8749.1985.tb04571.x.
PDF Share
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.