Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Neuroradiology
Published in: Neuroradiology 6/2010

Open Access 01-06-2010 | Topic Article

Patterns of neonatal hypoxic–ischaemic brain injury

Authors: Linda S. de Vries, Floris Groenendaal

Published in: Neuroradiology | Issue 6/2010

Login to get access

Abstract

Enormous progress has been made in assessing the neonatal brain, using magnetic resonance imaging (MRI). In this review, we will describe the use of MRI and proton magnetic resonance spectroscopy in detecting different patterns of brain injury in (full-term) human neonates following hypoxic–ischaemic brain injury and indicate the relevance of these findings in predicting neurodevelopmental outcome.
Literature
1.
Ranck JB, Windle WF (1959) Brain damage in the monkey, Macaca mulatta, by asphyxia neonatorum. Exp Neurol 1:130–154CrossRefPubMed
2.
Myers RE (1997) Two patterns of perinatal brain damage and their conditions of occurrence. Am J Obstet Gynecol 112:246–276
3.
Okereafor A, Allsop J, Counsell SJ, Fitzpatrick J, Azzopardi D, Rutherford MA, Cowan FM (2008) Patterns of brain injury in neonates exposed to perinatal sentinel events. Pediatrics 121:906–914CrossRefPubMed
4.
Miller SP, Ramaswamy V, Michelson D, Barkovich AJ, Holshouser B, Wycliffe N et al (2005) Patterns of brain injury in term neonatal encephalopathy. J Pediatr 146:453–460CrossRefPubMed
5.
Triulzi F, Parazzini C, Righini A (2006) Patterns of damage in the mature neonatal brain. Pediatr Radiol 36:608–620CrossRefPubMed
6.
Cady EB, Costello AM, Dawson MJ, Delpy DT, Hope PL, Reynolds EO et al (1983) Non-invasive investigation of cerebral metabolism in newborn infants by phosphorus nuclear magnetic resonance spectroscopy. Lancet 1:1059–1062CrossRefPubMed
7.
Younkin DP, Delivoria-Papadopoulos M, Leonard JC, Subramanian VH, Eleff S, Leigh JS Jr et al (1984) Unique aspects of human newborn cerebral metabolism evaluated with phosphorus nuclear magnetic resonance spectroscopy. Ann Neurol 16:581–586CrossRefPubMed
8.
Daneman A, Epelman M, Blaser S, Jarrin JR (2006) Imaging of the brain in full-term neonates: does sonography still play a role? Pediatr Radiol 36:636–646CrossRefPubMed
9.
Ment LR, Bada HS, Barnes P, Grant PE, Hirtz D, Papile LA et al (2002) Practice parameter: neuroimaging of the neonate: report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society. Neurology 58:1726–1738PubMed
10.
Perrin RG, Rutka JT, Drake JM, Meltzer H, Hellman J, Jay V et al (1997) Management and outcomes of posterior fossa subdural hematomas in neonates. Neurosurgery 40:1190–1199, discussion 1199–200CrossRefPubMed
11.
Brouwer AJ, Groenendaal F, Koopman C, Nievelstein RJ, Han KS, de Vries LS. Intracranial hemorrhage in full-term newborns: a hospital-based cohort study. Neuroradiology (in press)
12.
Pasternak JF, Gorey MT (1998) The syndrome of acute near-total intrauterine asphyxia in the term infant. Pediatr Neurol 18:391–398CrossRefPubMed
13.
Cowan F, Rutherford M, Groenendaal F, Eken P, Mercuri E, Bydder GM et al (2003) Origin and timing of brain lesions in term infants with neonatal encephalopathy. Lancet 361:736–742CrossRefPubMed
14.
Leijser LM, de Vries LS, Rutherford MA, Manzur AY, Groenendaal F, de Koning TJ et al (2007) Cranial ultrasound in metabolic disorders presenting in the neonatal period: characteristic features and comparison with MR imaging. AJNR Am J Neuroradiol 28:1223–1231CrossRefPubMed
15.
McKinstry RC, Miller JH, Snyder AZ, Mathur A, Schefft GL, Almli CR et al (2002) A prospective, longitudinal diffusion tensor imaging study of brain injury in newborns. Neurology 24(59):824–833
16.
Liauw L, van Wezel-Meijler G, Veen S, van Buchem MA, van der Grond J (2009) Do apparent diffusion coefficient measurements predict outcome in children with neonatal hypoxic–ischemic encephalopathy? AJNR Am J Neuroradiol 30:264–270CrossRefPubMed
17.
Malik GK, Trivedi R, Gupta RK, Hasan KM, Hasan M, Gupta A et al (2006) Serial quantitative diffusion tensor MRI of the term neonates with hypoxic–ischemic encephalopathy (HIE). Neuropediatrics 37:337–343CrossRefPubMed
18.
Soul JS, Robertson RL, Tzika AA, du Plessis AJ, Volpe JJ (2001) Time course of changes in diffusion-weighted magnetic resonance imaging in a case of neonatal encephalopathy with defined onset and duration of hypoxic–ischemic insult. Pediatrics 108:1211–1214CrossRefPubMed
19.
Barkovich AJ, Miller SP, Bartha A, Newton N, Hamrick SE, Mukherjee P et al (2006) MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy. AJNR Am J Neuroradiol 27:533–547PubMed
20.
Perlman JM (2003) Intrapartum asphyxia and cerebral palsy: is there a link? Clin Perinatol 33:335–353CrossRef
21.
Rutherford MA, Pennock JM, Counsell SJ, Mercuri E, Cowan FM, Dubowitz LM et al (1998) Abnormal magnetic resonance signal in the internal capsule predicts poor neurodevelopmental outcome in infants with hypoxic–ischemic encephalopathy. Pediatrics 102:323–328CrossRefPubMed
22.
Rutherford M, Counsell S, Allsop J, Boardman J, Kapellou O, Larkman D et al (2004) Diffusion-weighted magnetic resonance imaging in term perinatal brain injury: a comparison with site of lesion and time from birth. Pediatrics 114:1004–1014CrossRefPubMed
23.
Hunt RW, Neil JJ, Coleman LT, Kean MJ, Inder TE (2004) Apparent diffusion coefficient in the posterior limb of the internal capsule predicts outcome after perinatal asphyxia. Pediatrics 114:999–1003CrossRefPubMed
24.
Ward P, Counsell S, Allsop J, Cowan F, Shen Y, Edwards D, Rutherford M (2006) Reduced fractional anisotropy on diffusion tensor magnetic resonance imaging after hypoxic–ischemic encephalopathy. Pediatrics 117:e619–e630CrossRefPubMed
25.
Himmelmann K, Hagberg G, Wiklund LM, Eek MN, Uvebrant P (2007) Dyskinetic cerebral palsy: a population-based study of children born between 1991 and 1998. Dev Med Child Neurol 49:246–251CrossRefPubMed
26.
Groenendaal F, de Vries LS (2005) Watershed infarcts in the full term neonatal brain. Arch Dis Child Fetal Neonatal Ed 90:F488CrossRefPubMed
27.
Chau V, Poskitt KJ, Sargent MA, Lupton BA, Hill A, Roland E, Miller SP (2009) Comparison of computer tomography and magnetic resonance imaging scans on the third day of life in term newborns with neonatal encephalopathy. Pediatrics 123:319–326CrossRefPubMed
28.
Rutherford M, Pennock J, Schwieso J, Cowan F, Dubowitz L (1996) Hypoxic-ischaemic encephalopathy: early and late magnetic resonance imaging findings in relation to outcome. Arch Dis Child Fetal Neonatal Ed 75:F145–F151CrossRefPubMed
29.
Burns C, Boardman J, Rutherford M et al (2008) Patterns of cerebral injury and neurodevelopmental outcome following symptomatic neonatal hypoglycaemia. Pediatrics 122:65–74CrossRefPubMed
30.
Sato Y, Hayakawa M, Iwata O, Okumura A, Kato T, Hayakawa F et al (2008) Delayed neurological signs following isolated parasagittal injury in asphyxia at term. Eur J Paediatr Neurol 12:359–365CrossRefPubMed
31.
Mercuri E, Ricci D, Cowan FM, Lessing D, Frisone MF, Haataja L et al (2000) Head growth in infants with hypoxic–ischemic encephalopathy: correlation with neonatal magnetic resonance imaging. Pediatrics 106:235–243CrossRefPubMed
32.
Steinman KJ, Gorno-Tempini ML, Glidden DV, Kramer JH, Miller SP, Barkovich AJ, Ferriero DM (2009) Neonatal watershed brain injury on magnetic resonance imaging correlates with verbal IQ at 4 years. Pediatrics 123:1025–1030CrossRefPubMed
33.
Miller SP, Ferriero NN, DM PJC, Glidden DV, Barnwell A et al (2002) Predictors of 30-month outcome after perinatal depression: role of proton MRS and socioeconomic factors. Pediatr Res 52:71–77CrossRefPubMed
34.
Oguni H, Sugama M, Osawa M (2008) Symptomatic parieto-occipital epilepsy as sequela of perinatal asphyxia. Pediatr Neurol 38:345–352CrossRefPubMed
35.
Vermeulen RJ, Fetter WP, Hendrikx L, Van Schie PE, van der Knaap MS, Barkhof F (2003) Diffusion-weighted MRI in severe neonatal hypoxic ischaemia: the white cerebrum. Neuropediatrics 34:72–76CrossRefPubMed
36.
Dodelson DK, Grosso C (2005) Maternal mutation 677C>T in the ethylenetetrahydrofolate reductase gene associated with severe brain injury in offspring. Clin Genet 67:69–80CrossRef
37.
Li AM, Chau V, Poskitt KJ, Sargent MA, Lupton BA, Hill A et al (2009) White matter injury in term newborns with neonatal encephalopathy. Pediatr Res 65:85–89CrossRefPubMed
38.
Galli KK, Zimmerman RA, Jarvik GP, Wernovsky G, Kuypers MK, Clancy RR et al (2004) Periventricular leukomalacia is common after neonatal cardiac surgery. J Thorac Cardiovasc Surg 127:692–704CrossRefPubMed
39.
Ramaswamy V, Miller SP, Barkovich AJ, Partridge JC, Ferriero DM (2004) Perinatal stroke in term infants with neonatal encephalopathy. Neurology 62:2088–2091PubMed
40.
Cheong JL, Cowan FM (2009) Neonatal arterial ischaemic stroke: obstetric issues. Semin Fetal Neonatal Med 14:267–271CrossRefPubMed
41.
Cowan F, Mercuri E, Groenendaal F, Bassi L, Ricci D, Rutherford M, de Vries LS (2005) Does cranial ultrasound imaging identify arterial cerebral infarction in term neonates? Arch Dis Child Fetal Neonatal Ed 90:F252–F256CrossRefPubMed
42.
De Vries LS, Van der Grond J, Van Haastert IC, Groenendaal F (2005) Prediction of outcome in new-born infants with arterial ischaemic stroke using diffusion-weighted magnetic resonance imaging. Neuropediatrics 36:12–20CrossRefPubMed
43.
Kirton A, Shroff M, Visvanathan T, deVeber G (2007) Quantified corticospinal tract diffusion restriction predicts neonatal stroke outcome. Stroke 38:974–980CrossRefPubMed
44.
Lequin MH, Dudink J, Tong KA, Obenaus A (2009) Magnetic resonance imaging in neonatal stroke. Semin Fetal Neonatal Med 14:299–310CrossRefPubMed
45.
Glenn OA, Ludeman NA, Berman JI, Wu YW, Lu Y, Bartha AI et al (2007) Diffusion tensor MR imaging tractography of the pyramidal tracts correlates with clinical motor function in children with congenital hemiparesis. AJNR Am J Neuroradiol 28:1796–1802CrossRefPubMed
46.
Ashwal S, Obenaus A, Snyder EY (2009) Neuroimaging as a basis for rational stem cell therapy. Pediatr Neurol 40:227–236CrossRefPubMed
47.
Staudt M, Grodd W, Gerloff C, Erb M, Stitz J, Krägeloh-Mann I (2002) Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study. Brain 125:2222–2237CrossRefPubMed
48.
Seghier ML, Lazeyras F, Zimine S, Saudan-Frei S, Safran AB, Huppi PS (2005) Visual recovery after perinatal stroke evidenced by functional and diffusion MRI: case report. BMC Neurol 26(5):17CrossRef
49.
Arichi T, Moraux A, Melendez A, Doria V, Groppo M, Merchant N et al (2009) Somatosensory cortical activation identified by functional MRI in preterm and term infants. Neuroimage 49(3):2063–2071CrossRefPubMed
50.
Heep A, Scheef L, Jankowski J, Born M, Zimmermann N, Sival D et al (2009) Functional magnetic resonance imaging of the sensorimotor system in preterm infants. Pediatrics 123:294–300CrossRefPubMed
51.
Armstrong-Wells J, Johnston SC, Wu YW, Sidney S, Fullerton HJ (2009) Prevalence and predictors of perinatal hemorrhagic stroke: results from the Kaiser Pediatric Stroke Study. Pediatrics 123:823–828CrossRefPubMed
52.
deVeber G, Andrew M, Adams C, Bjornson B, Booth F, Buckley DJ et al (2001) Cerebral sinovenous thrombosis in children. N Engl J Med 345:417–423CrossRefPubMed
53.
Wu YW, Miller SP, Chin K, Collins AE, Lomeli SC, Chuang NA et al (2002) Multiple risk factors in neonatal sinovenous thrombosis. Neurology 59:438–440PubMed
54.
Kersbergen KJ, de Vries LS, van Straaten HL, Benders MJ, Nievelstein RA, Groenendaal F (2009) Anticoagulation therapy and imaging in neonates with a unilateral thalamic hemorrhage due to cerebral sinovenous thrombosis. Stroke 40:2754–2760CrossRefPubMed
55.
Govaert P, Voet D, Achten E, Vanhaesebrouck P, van Rostenberghe H, van Gysel D et al (1992) Noninvasive diagnosis of superior sagittal sinus thrombosis in a neonate. Am J Perinatol 9:201–204CrossRefPubMed
56.
Tsao PN, Lee WT, Peng SF, Lin JH, Yau KI (1999) Power Doppler ultrasound imaging in neonatal cerebral venous sinus thrombosis. Pediatr Neurol 21:652–655CrossRefPubMed
57.
Davies RP, Slavotinek JP (1994) Incidence of the empty delta sign in computed tomography in the paediatric age group. Australas Radiol 38:17–19CrossRefPubMed
58.
Eichler F, Krishnamoorthy K, Grant PE (2007) Magnetic resonance imaging evaluation of possible neonatal sinovenous thrombosis. Pediatr Neurol 37:317–323CrossRefPubMed
59.
Takekawa H, Tanaka H, Ogawa T, Niijima Y, Sada T, Daimon Y et al (2008) Usefulness of echo-planar T2* susceptibility-weighted imaging for reliable diagnosis of cerebral venous sinus thrombosis. Intern Med 47:2101–2102CrossRefPubMed
60.
Kawabori M, Kuroda S, Kudo K, Terae S, Kaneda M, Nakayama N et al (2009) Susceptibility-weighted magnetic resonance imaging detects impaired cerebral hemodynamics in the superior sagittal sinus thrombosis—case report. Neurol Med Chir (Tokyo) 49:248–251CrossRef
61.
Petroff OA, Prichard JW, Behar KL, Rothman DL, Alger JR, Shulman RG (1985) Cerebral intracellular pH by 31P nuclear magnetic resonance spectroscopy. Neurology 35:781–788PubMed
62.
van der Knaap MS, van der Grond J, van Rijen PC, Faber JA, Valk J, Willemse K (1990) Age-dependent changes in localized proton and phosphorus MR spectroscopy of the brain. Radiology 176:509–515PubMed
63.
Younkin DP, Wagerle LC, Chance B, Maria J, Delivoria-Papadopoulos M (1987) 31P-NMR studies of cerebral metabolic changes during graded hypoxia in newborn lambs. J Appl Physiol 62:1569–1574PubMed
64.
Hope PL, Costello AM, Cady EB, Delpy DT, Tofts PS, Chu A et al (1984) Cerebral energy metabolism studied with phosphorous NMR spectroscopy in normal and birth asphyxiated infants. Lancet 8399:366–370CrossRef
65.
Wyatt JS, Edwards AD, Azzopardi D, Reynolds EO (1989) Magnetic resonance and near infrared spectroscopy for investigation of perinatal hypoxic–ischaemic brain injury. Arch Dis Child 64:953–963CrossRefPubMed
66.
Moorcraft J, Bolas NM, Ives NK, Ouwerkerk R, Smyth J, Rajagopalan B et al (1991) Global and depth resolved phosphorus magnetic resonance spectroscopy to predict outcome after birth asphyxia. Arch Dis Child 66:1119–1123CrossRefPubMed
67.
Roth SC, Edwards AD, Cady EB, Delpy DT, Wyatt JS, Azzopardi D et al (1992) Relation between cerebral oxidative metabolism following birth asphyxia, and neurodevelopmental outcome and brain growth at one year. Dev Med Child Neurol 34:285–295PubMedCrossRef
68.
Lorek A, Takei Y, Cady EB, Wyatt JS, Penrice J, Edwards AD et al (1994) Delayed (“secondary”) cerebral energy failure after acute hypoxia-ischemia in the newborn piglet: continuous 48-hour studies by phosphorus magnetic resonance spectroscopy. Pediatr Res 36:699–706CrossRefPubMed
69.
Penrice J, Lorek A, Cady EB, Amess PN, Wylezinska M, Cooper CE et al (1997) Proton magnetic resonance spectroscopy of the brain during acute hypoxia–ischemia and delayed cerebral energy failure in the newborn piglet. Pediatr Res 41:795–802CrossRefPubMed
70.
Groenendaal F, de Graaf RA, van Vliet G, Nicolay K (1999) Effects of hypoxia–ischemia and inhibition of nitric oxide synthase on cerebral energy metabolism in newborn piglets. Pediatr Res 45:827–833CrossRefPubMed
71.
Amess PN, Penrice J, Cady EB, Lorek A, Wylezinska M, Cooper CE et al (1997) Mild hypothermia after severe transient hypoxia–ischemia reduces the delayed rise in cerebral lactate in the newborn piglet. Pediatr Res 41:803–808CrossRefPubMed
72.
Peeters-Scholte C, Koster JG, Veldhuis W, van den Tweel E, Zhu C, Kops N et al (2002) Neuroprotection by selective nitric oxide synthase inhibition at 24 hours after perinatal hypoxia–ischemia. Stroke 33:2304–2310CrossRefPubMed
73.
Peden CJ, Cowan FM, Bryant DJ, Sargentoni J, Cox IJ, Menon DK et al (1990) Proton MR spectroscopy of the brain in infants. J Comput Assist Tomogr 14:886–894CrossRefPubMed
74.
Toft PB, Leth H, Lou H, Pryds O, Henriksen O (1994) Metabolite concentrations in the developing brain estimated with proton MR spectroscopy. J Magn Reson Imaging 4:674–680CrossRefPubMed
75.
Groenendaal F, Veenhoven RH, van der Grond J, Jansen GH, Witkamp TD, de Vries LS (1994) Cerebral lactate and N-acetyl-aspartate/choline ratios in asphyxiated full-term neonates demonstrated in vivo using proton magnetic resonance spectroscopy. Pediatr Res 35:148–151CrossRefPubMed
76.
Roelants-van Rijn AM, van der Grond J, Stigter RH, de Vries LS, Groenendaal F (2004) Cerebral structure and metabolism, and long-term outcome in small-for-gestational-age preterm neonates. Pediatr Res 56:285–290CrossRefPubMed
77.
Leth H, Toft PB, Pryds O, Peitersen B, Lou HC, Henriksen O (1995) Brain lactate in preterm and growth-retarded neonates. Acta Paediatr 84:495–499CrossRefPubMed
78.
Robertson NJ, Cox IJ, Cowan FM, Counsell SJ, Azzopardi D, Edwards AD (1999) Cerebral intracellular lactic alkalosis persisting months after neonatal encephalopathy measured by magnetic resonance spectroscopy. Pediatr Res 46:287–296CrossRefPubMed
79.
Groenendaal F, van der Grond J, Witkamp TD, de Vries LS (1995) Proton magnetic resonance spectroscopic imaging in neonatal stroke. Neuropediatrics 26:243–248CrossRefPubMed
80.
Roelants-van Rijn AM, van der Grond J, de Vries LS, Groenendaal F (2001) Value of 1H-MRS using different echo times in neonates with cerebral hypoxia–ischemia. Pediatr Res 49:356–362CrossRefPubMed
81.
Thayyil S, Chandrasekaran M, Taylor A, Bainbridge A, Cady EB, Chong WK et al (2010) Cerebral magnetic resonance biomarkers in neonatal encephalopathy: a meta-analysis. Pediatrics 125:e382–e395CrossRefPubMed
82.
L'Abee C, de Vries LS, van der Grond J, Groenendaal F (2005) Early diffusion-weighted MRI and 1H-magnetic resonance spectroscopy in asphyxiated fullterm neonates. Biol Neonate 88:306–312CrossRefPubMed
Metadata
Title
Patterns of neonatal hypoxic–ischaemic brain injury
Authors
Linda S. de Vries
Floris Groenendaal
Publication date
01-06-2010
Publisher
Springer-Verlag
Published in
Neuroradiology / Issue 6/2010
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-010-0674-9

Other articles of this Issue 6/2010

Neuroradiology 6/2010 Go to the issue

Topic Article

Congenital tumors of the central nervous system

Topic Article

The corpus callosum, the other great forebrain commissures, and the septum pellucidum: anatomy, development, and malformation

Topic Article

Intracranial hemorrhage in full-term newborns: a hospital-based cohort study

Paediatric Neuroradiology

Neuroimaging findings in pediatric Wernicke encephalopathy: a review

Topic Article

Forebrain development in fetal MRI: evaluation of anatomical landmarks before gestational week 27

Topic Article

Common and unusual craniofacial manifestations of metastatic neuroblastoma