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Open Access 01-12-2020 | Magnetic Resonance Imaging | Educational Review

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

Authors: Anith Chacko, Savvas Andronikou, Ali Mian, Fabrício Guimarães Gonçalves, Schadie Vedajallam, Ngoc Jade Thai

Published in: Insights into Imaging | Issue 1/2020

Abstract

The inter-arterial watershed zone in neonates is a geographic area without discernible anatomic boundaries and difficult to demarcate and usually not featured in atlases. Schematics currently used to depict the areas are not based on any prior anatomic mapping, compared to adults.

Magnetic resonance imaging (MRI) of neonates in the acute to subacute phase with suspected hypoxic-ischaemic injury (HII) can demonstrate signal abnormality and restricted diffusion in the cortical and subcortical parenchyma of the watershed regions.

In the chronic stage of partial-prolonged hypoxic-ischaemic injury, atrophy and ulegyria can make the watershed zone more conspicuous as a region. Our aim is to use images extracted from a sizable medicolegal database (approximately 2000 cases), of delayed MRI scans in children with cerebral palsy, to demonstrate the watershed region.

To achieve this, we have selected cases diagnosed on imaging as having sustained a term pattern of partial-prolonged HII affecting the hemispheric cortex, based on the presence of bilateral, symmetric atrophy with ulegyria. From these, we have identified those patients demonstrating injury along the whole watershed continuum as well as those demonstrating selective anterior or posterior watershed predominant injury for demonstration.

Recognition of this zone is essential for diagnosing partial-prolonged hypoxic-ischaemic injury sustained in term neonates. The images presented in this pictorial review provide a template for identifying the cortical watershed distribution when there is milder regional (anterior, parasagittal, peri-Sylvian and posterior) watershed injury and for more severe injury where multiple regions are injured in combination or as a continuum.

Gunn AJ, Bennet L (2009) Fetal hypoxia insults and patterns of brain injury: insights from animal models. Clin Perinatol 36:579–593. https://doi.org/10.1016/j.clp.2009.06.007 CrossRefPubMedPubMedCentral

Bano S, Chaudhary V, Garga UC et al (2017) Neonatal hypoxic-ischaemic encephalopathy: a radiological review. J Pediatr Neurosci 12:1–6. https://doi.org/10.4103/1817-1745.205646

Chao CP, Zaleski CG, Patton AC et al (2006) Neonatal hypoxic-ischaemic encephalopathy: multimodality imaging findings. Radiographics 26 Suppl 1:S159-S172 https://doi.org/10.1148/rg.26si065504.

Shroff MM, Soares-Fernandes JP, Whyte H et al (2010) MR imaging for diagnostic evaluation of encephalopathy in the newborn. Radiographics 30:763–780. https://doi.org/10.1148/rg.303095126

Ferriero DM (2004) Neonatal brain injury. N Engl J Med 351:1985–1995. https://doi.org/10.1056/NEJMra041996 CrossRefPubMed

Nikas I, Dermentzoglou V, Theofanopoulou M et al (2008) Parasagittal lesions and ulegyria in hypoxic-ischaemic encephalopathy: neuroimaging findings and review of the pathogenesis. J Child Neurol 23:51–58. https://doi.org/10.1177/0883073807308694

Johnston MV, Trescher WH, Ishida A et al (2001) Neurobiology of hypoxic-ischaemic injury in the developing brain. Pediatr Res 49:735–741. https://doi.org/10.1203/00006450-200106000-00003

Shalak L, Perlman JM (2004) Hypoxic-ischaemic brain injury in the term infant-current concepts. Early Hum Dev 80:125–141. https://doi.org/10.1016/j.earlhumdev.2004.06.003 CrossRefPubMed

Merchant N, Azzopardi D (2015) Early predictors of outcome in infants treated with hypothermia for hypoxic-ischaemic encephalopathy. Dev Med Child Neurol 57(Suppl 3):8–16. https://doi.org/10.1111/dmcn.12726 CrossRefPubMed

10.

Srinivasakumar P, Zempel J, Wallendorf M et al (2013) Therapeutic hypothermia in neonatal hypoxic ischemic encephalopathy: electrographic seizures and magnetic resonance imaging evidence of injury. J Pediatr 163:465–470. https://doi.org/10.1016/j.jpeds.2013.01.041

11.

Inder TE, Hunt RW, Morley CJ et al (2004) Randomized trial of systemic hypothermia selectively protects the cortex on MRI in term hypoxic-ischaemic encephalopathy. J Pediatr 145:835–837. https://doi.org/10.1016/j.jpeds.2004.07.034

12.

Rutherford M, Ramenghi LA, Edwards AD et al (2010) Assessment of brain tissue injury after moderate hypothermia in neonates with hypoxic-ischaemic encephalopathy: a nested substudy of a randomised controlled trial. Lancet Neurol 9:39–45. https://doi.org/10.1016/S1474-4422(09)70295-9

13.

Volpe JJ, Inder TE, Darras BT et al (2017) Volpe’s Neurology of the Newborn. Saunders Ltd, Philadelphia

14.

Rutherford M, Srinivasan L, Dyet L et al (2006) Magnetic resonance imaging in perinatal brain injury: clinical presentation, lesions and outcome. Pediatr Radiol 36:582–592. https://doi.org/10.1007/s00247-006-0164-8

15.

Kuker W, Mohrle S, Mader I et al (2004) MRI for the management of neonatal cerebral infarctions: importance of timing. Childs Nerv Syst 20:742–748. https://doi.org/10.1007/s00381-004-0988-1

16.

Mader I, Schoning M, Klose U et al (2002) Neonatal cerebral infarction diagnosed by diffusion-weighted MRI: pseudonormalization occurs early. Stroke 33:1142–1145. https://doi.org/10.1161/hs0402.105883

17.

Perez A, Ritter S, Brotschi B et al (2013) Long-term neurodevelopmental outcome with hypoxic-ischaemic encephalopathy. J Pediatr 163:454–459. https://doi.org/10.1016/j.jpeds.2013.02.003

18.

Miller SP, Ramaswamy V, Michelson Det al (2005) Patterns of brain injury in term neonatal encephalopathy. J Pediatr 146:453–460. https://doi.org/10.1016/j.jpeds.2004.12.026

19.

Steinman KJ, Gorno-Tempini ML, Glidden DV et al (2009) Neonatal watershed brain injury on magnetic resonance imaging correlates with verbal IQ at 4 years. Pediatrics 123:1025–1030. https://doi.org/10.1542/peds.2008-1203

20.

de Vries LS, Jongmans MJ (2010) Long-term outcome after neonatal hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 95:F220–F224. https://doi.org/10.1136/adc.2008.148205 CrossRefPubMed

21.

Kim DE, Park JH, Schellingerhout D et al (2019) Mapping the supratentorial cerebral arterial territories using 1160 large artery infarcts. JAMA Neurol 76:72–80. https://doi.org/10.1001/jamaneurol.2018.2808

22.

de Vries LS, Cowan FM (2009) Evolving understanding of hypoxic-ischaemic encephalopathy in the term infant. Semin Pediatr Neurol 16:216–225. https://doi.org/10.1016/j.spen.2009.09.001 CrossRefPubMed

23.

Cowan F, Rutherford M, Groenendaal F et al (2003) Origin and timing of brain lesions in term infants with neonatal encephalopathy. Lancet 361:736-742 doi:https://doi.org/10.1016/s0140-6736(03)12658-x.

24.

Huang BY, Castillo M (2008) hypoxic-ischaemic brain injury: imaging findings from birth to adulthood. Radiographics 28:417–439; quiz 617. https://doi.org/10.1148/rg.282075066

25.

Bydder GM, Rutherford MA (2001) Diffusion-weighted imaging of the brain in neonates and infants. Magn Reson Imaging Clin N Am 9:83-98, viii.

26.

Bydder GM, Rutherford MA, Cowan FM et al (2001) Diffusion-weighted imaging in neonates. Childs Nerv Syst 17:190–194

27.

Dyet LE, Kennea N, Counsell SJ et al (2006) Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118:536–548. https://doi.org/10.1542/peds.2005-1866

28.

Simpson E, Andronikou S, Vedajallam S et al (2016) Curved reformat of the paediatric brain MRI into a 'flat-earth map' - standardised method for demonstrating cortical surface atrophy resulting from hypoxic-ischaemic encephalopathy. Pediatr Radiol 46:1482–1488. https://doi.org/10.1007/s00247-016-3638-3

29.

Ghei SK, Zan E, Nathan JE et al (2014) MR imaging of hypoxic-ischaemic injury in term neonates: pearls and pitfalls. Radiographics 34:1047–1061. https://doi.org/10.1148/rg.344130080

30.

Huppi PS, Murphy B, Maier SEet al (2001) Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 107:455–460

31.

Krishnan P, Shroff M (2016) Neuroimaging in neonatal hypoxic ischemic encephalopathy. Indian J Pediatr. https://doi.org/10.1007/s12098-016-2042-1

32.

Rutherford MA, Pennock J, Schwieso J et al (1996) Hypoxic-ischaemic encephalopathy: early and late magnetic resonance imaging findings in relation to outcome. Arch Dis Child Fetal Neonatal Ed 75:F145–F151

33.

Barkovich AJ, Miller SP, Bartha A et al (2006) MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy. AJNR Am J Neuroradiol 27:533–547

34.

Volpe JJ (2012) Neonatal encephalopathy: an inadequate term for hypoxic-ischaemic encephalopathy. Ann Neurol 72:156–166. https://doi.org/10.1002/ana.23647 CrossRefPubMed

35.

Prabhhu S, Andronikou S, Vargas SO et al (2017) Paediatric neuroradiology - brain. In: Lee EY (ed) Pediatric radiology: practical imaging evaluation of infants and children. Lippincott Williams and Wilkins, Philadelphia

36.

Villani F, D'Incerti L, Granata T et al (2003) Epileptic and imaging findings in perinatal hypoxic-ischaemic encephalopathy with ulegyria. Epilepsy Res 55:235–243

37.

Norman MG (1981) On the morphogenesis of ulegyria. Acta Neuropathol 53:331–332. https://doi.org/10.1007/bf00690375 CrossRefPubMed

38.

Mangla R, Kolar B, Almast J et al (2011) Border zone infarcts: pathophysiologic and imaging characteristics. Radiographics 31:1201–1214. https://doi.org/10.1148/rg.315105014

39.

Hill A, Volpe JJ (1985) Pathogenesis and management of hypoxic-ischaemic encephalopathy in the term newborn. Neurol Clin 3:31–46CrossRef

40.

Burns CM, Rutherford MA, Boardman JP et al (2008) Patterns of cerebral injury and neurodevelopmental outcomes after symptomatic neonatal hypoglycemia. Pediatrics 122:65–74. https://doi.org/10.1542/peds.2007-2822

41.

Andronikou S, Ackermann C, Laughton B et al (2015) Corpus callosum thickness on mid-sagittal MRI as a marker of brain volume: a pilot study in children with HIV-related brain disease and controls. Pediatr Radiol 45:1016–1025. https://doi.org/10.1007/s00247-014-3255-y

42.

Andronikou S, Pillay T, Gabuza L et al (2015) Corpus callosum thickness in children: an MR pattern-recognition approach on the midsagittal image. Pediatr Radiol 45:258–272. https://doi.org/10.1007/s00247-014-2998-9

43.

Mercuri E, Dubowitz L, Rutherford MA et al (2001) Cerebral infarction in the full-term infant. In: Rutherford MA (ed) MRI of the neonatal brain. Saunders Ltd.

Title: 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
Authors: Anith Chacko
Savvas Andronikou
Ali Mian
Fabrício Guimarães Gonçalves
Schadie Vedajallam
Ngoc Jade Thai
Publication date: 01-12-2020
Publisher: Springer Berlin Heidelberg
Keywords: Magnetic Resonance Imaging
Magnetic Resonance Imaging
Published in: Insights into Imaging / Issue 1/2020
Electronic ISSN: 1869-4101
DOI: https://doi.org/10.1186/s13244-020-00857-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

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

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

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