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Semin Neurol 2020; 40(03): 322-334
DOI: 10.1055/s-0040-1702939
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Predictors of Long-Term Neurodevelopmental Outcome of Hypoxic-Ischemic Encephalopathy Treated with Therapeutic Hypothermia

Ipsita Goswami  ‡   *
1   Department of Paediatrics, Hospital for Sick Children, Toronto, Canada
2   Department of Paediatrics, University of Toronto, Toronto, Canada
,
Mireille Guillot‡   *
1   Department of Paediatrics, Hospital for Sick Children, Toronto, Canada
2   Department of Paediatrics, University of Toronto, Toronto, Canada
,
Emily W. Y. Tam
1   Department of Paediatrics, Hospital for Sick Children, Toronto, Canada
2   Department of Paediatrics, University of Toronto, Toronto, Canada
› Author Affiliations
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Publication History

Publication Date:
20 February 2020 (online)

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Abstract

Hypoxic-ischemic encephalopathy (HIE) is a manifestation of perinatal asphyxial insult that continues to evolve over days to weeks following the initial injury. Therapeutic hypothermia has demonstrated that a proportion of this secondary brain injury may indeed be preventable. However, therapeutic hypothermia has also altered the prognostic utility of many bedside tools that are commonly used as predictors of long-term neurodevelopmental outcome in HIE. Clinicians are often confronted with uncertainty when assessing the prognosis of infants with HIE. Improved understanding of the implications and limitations of individual investigations may inform clinical decisions and allow for timely intervention. This review summarizes the predictive value of currently available prognostic markers in HIE infants in the therapeutic hypothermia era, including clinical, biochemical, neurophysiological, physiological, and neuroimaging predictors.

Keywords

Hypoxic-ischemic encephalopathy - therapeutic hypothermia - neurodevelopmental outcome - electroencephalography - magnetic resonance imaging

* Both these authors contributed equally to the manuscript.


 

  • References

  • 1 Executive summary: Neonatal encephalopathy and neurologic outcome, second edition. Report of the American College of Obstetricians and Gynecologists' Task Force on Neonatal Encephalopathy. Obstet Gynecol 2014; 123 (04) 896-901
    CrossrefPubMedGoogle Scholar
  • 2 Kurinczuk JJ, White-Koning M, Badawi N. Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum Dev 2010; 86 (06) 329-338
    CrossrefPubMedGoogle Scholar
  • 3 Rasmussen LA, Cascio MA, Ferrand A, Shevell M, Racine E. The complexity of physicians' understanding and management of prognostic uncertainty in neonatal hypoxic-ischemic encephalopathy. J Perinatol 2019; 39 (02) 278-285
    CrossrefPubMedGoogle Scholar
  • 4 Samejima K, Toné S, Kottke TJ. , et al. Transition from caspase-dependent to caspase-independent mechanisms at the onset of apoptotic execution. J Cell Biol 1998; 143 (01) 225-239
    CrossrefPubMedGoogle Scholar
  • 5 Wassink G, Gunn ER, Drury PP, Bennet L, Gunn AJ. The mechanisms and treatment of asphyxial encephalopathy. Front Neurosci 2014; 8: 40
    PubMedGoogle Scholar
  • 6 Polderman KH. Mechanisms of action, physiological effects, and complications of hypothermia. Crit Care Med 2009; 37 (7, Suppl): S186-S202
    CrossrefPubMedGoogle Scholar
  • 7 Nakashima K, Todd MM. Effects of hypothermia on the rate of excitatory amino acid release after ischemic depolarization. Stroke 1996; 27 (05) 913-918
    CrossrefPubMedGoogle Scholar
  • 8 Mueller-Burke D, Koehler RC, Martin LJ. Rapid NMDA receptor phosphorylation and oxidative stress precede striatal neurodegeneration after hypoxic ischemia in newborn piglets and are attenuated with hypothermia. Int J Dev Neurosci 2008; 26 (01) 67-76
    CrossrefPubMedGoogle Scholar
  • 9 Fukui O, Kinugasa Y, Fukuda A. , et al. Post-ischemic hypothermia reduced IL-18 expression and suppressed microglial activation in the immature brain. Brain Res 2006; 1121 (01) 35-45
    CrossrefPubMedGoogle Scholar
  • 10 Xiong M, Yang Y, Chen GQ, Zhou WH. Post-ischemic hypothermia for 24h in P7 rats rescues hippocampal neuron: association with decreased astrocyte activation and inflammatory cytokine expression. Brain Res Bull 2009; 79 (06) 351-357
    CrossrefPubMedGoogle Scholar
  • 11 Wang GJ, Deng HY, Maier CM, Sun GH, Yenari MA. Mild hypothermia reduces ICAM-1 expression, neutrophil infiltration and microglia/monocyte accumulation following experimental stroke. Neuroscience 2002; 114 (04) 1081-1090
    CrossrefPubMedGoogle Scholar
  • 12 Laptook AR, Corbett RJ, Sterett R, Burns DK, Garcia D, Tollefsbol G. Modest hypothermia provides partial neuroprotection when used for immediate resuscitation after brain ischemia. Pediatr Res 1997; 42 (01) 17-23
    CrossrefPubMedGoogle Scholar
  • 13 Laptook AR, Corbett RJ, Burns DK, Sterett R. A limited interval of delayed modest hypothermia for ischemic brain resuscitation is not beneficial in neonatal swine. Pediatr Res 1999; 46 (04) 383-389
    CrossrefPubMedGoogle Scholar
  • 14 Gunn AJ, Bennet L, Gunning MI, Gluckman PD, Gunn TR. Cerebral hypothermia is not neuroprotective when started after postischemic seizures in fetal sheep. Pediatr Res 1999; 46 (03) 274-280
    CrossrefPubMedGoogle Scholar
  • 15 Shankaran S, Laptook AR, Pappas A. , et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Effect of depth and duration of cooling on deaths in the NICU among neonates with hypoxic ischemic encephalopathy: a randomized clinical trial. JAMA 2014; 312 (24) 2629-2639
    CrossrefPubMedGoogle Scholar
  • 16 Thoresen M, Satas S, Løberg EM. , et al. Twenty-four hours of mild hypothermia in unsedated newborn pigs starting after a severe global hypoxic-ischemic insult is not neuroprotective. Pediatr Res 2001; 50 (03) 405-411
    CrossrefPubMedGoogle Scholar
  • 17 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; (01) CD003311
    PubMedGoogle Scholar
  • 18 Edwards AD, Brocklehurst P, Gunn AJ. , et al. Neurological outcomes at 18 months of age after moderate hypothermia for perinatal hypoxic ischaemic encephalopathy: synthesis and meta-analysis of trial data. BMJ 2010; 340: c363
    CrossrefPubMedGoogle Scholar
  • 19 Tagin MA, Woolcott CG, Vincer MJ, Whyte RK, Stinson DA. Hypothermia for neonatal hypoxic ischemic encephalopathy: an updated systematic review and meta-analysis. Arch Pediatr Adolesc Med 2012; 166 (06) 558-566
    PubMedGoogle Scholar
  • 20 Srinivasakumar P, Zempel J, Wallendorf M, Lawrence R, Inder T, Mathur A. Therapeutic hypothermia in neonatal hypoxic ischemic encephalopathy: electrographic seizures and magnetic resonance imaging evidence of injury. J Pediatr 2013; 163 (02) 465-470
    CrossrefPubMedGoogle Scholar
  • 21 Orbach SA, Bonifacio SL, Kuzniewicz MW, Glass HC. Lower incidence of seizure among neonates treated with therapeutic hypothermia. J Child Neurol 2014; 29 (11) 1502-1507
    CrossrefPubMedGoogle Scholar
  • 22 Kapetanakis A, Azzopardi D, Wyatt J, Robertson NJ. Therapeutic hypothermia for neonatal encephalopathy: a UK survey of opinion, practice and neuro-investigation at the end of 2007. Acta Paediatr 2009; 98 (04) 631-635
    CrossrefPubMedGoogle Scholar
  • 23 Azzopardi D, Strohm B, Marlow N. , et al; TOBY Study Group. Effects of hypothermia for perinatal asphyxia on childhood outcomes. N Engl J Med 2014; 371 (02) 140-149
    CrossrefPubMedGoogle Scholar
  • 24 Shankaran S, Pappas A, McDonald SA. , et al; Eunice Kennedy Shriver NICHD Neonatal Research Network. Childhood outcomes after hypothermia for neonatal encephalopathy. N Engl J Med 2012; 366 (22) 2085-2092
    CrossrefPubMedGoogle Scholar
  • 25 Shankaran S, Laptook AR, Ehrenkranz RA. , et al; National Institute of Child Health and Human Development Neonatal Research Network. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med 2005; 353 (15) 1574-1584
    CrossrefPubMedGoogle Scholar
  • 26 Hayes BC, Doherty E, Grehan A. , et al. Neurodevelopmental outcome in survivors of hypoxic ischemic encephalopathy without cerebral palsy. Eur J Pediatr 2018; 177 (01) 19-32
    CrossrefPubMedGoogle Scholar
  • 27 Odd DE, Whitelaw A, Gunnell D, Lewis G. The association between birth condition and neuropsychological functioning and educational attainment at school age: a cohort study. Arch Dis Child 2011; 96 (01) 30-37
    CrossrefPubMedGoogle Scholar
  • 28 McDonough TL, Paolicchi JM, Heier LA. , et al. Prediction of future epilepsy in neonates with hypoxic-ischemic encephalopathy who received selective head cooling. J Child Neurol 2017; 32 (07) 630-637
    CrossrefPubMedGoogle Scholar
  • 29 Cannon TD, Rosso IM, Hollister JM, Bearden CE, Sanchez LE, Hadley T. A prospective cohort study of genetic and perinatal influences in the etiology of schizophrenia. Schizophr Bull 2000; 26 (02) 351-366
    CrossrefPubMedGoogle Scholar
  • 30 Gardener H, Spiegelman D, Buka SL. Perinatal and neonatal risk factors for autism: a comprehensive meta-analysis. Pediatrics 2011; 128 (02) 344-355
    CrossrefPubMedGoogle Scholar
  • 31 Laptook AR, Shankaran S, Ambalavanan N. , et al; Hypothermia Subcommittee of the NICHD Neonatal Research Network. Outcome of term infants using Apgar scores at 10 minutes following hypoxic-ischemic encephalopathy. Pediatrics 2009; 124 (06) 1619-1626
    CrossrefPubMedGoogle Scholar
  • 32 Natarajan G, Shankaran S, Laptook AR. , et al; Extended Hypothermia Subcommittee of the Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Apgar scores at 10 min and outcomes at 6-7 years following hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 2013; 98 (06) F473-F479
    CrossrefPubMedGoogle Scholar
  • 33 Sarkar S, Bhagat I, Dechert RE, Barks JD. Predicting death despite therapeutic hypothermia in infants with hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 2010; 95 (06) F423-F428
    CrossrefPubMedGoogle Scholar
  • 34 Shah P, Anvekar A, McMichael J, Rao S. Outcomes of infants with Apgar score of zero at 10 min: the West Australian experience. Arch Dis Child Fetal Neonatal Ed 2015; 100 (06) F492-F494
    CrossrefPubMedGoogle Scholar
  • 35 Kasdorf E, Laptook A, Azzopardi D, Jacobs S, Perlman JM. Improving infant outcome with a 10 min Apgar of 0. Arch Dis Child Fetal Neonatal Ed 2015; 100 (02) F102-F105
    CrossrefPubMedGoogle Scholar
  • 36 Wyatt JS, Gluckman PD, Liu PY. , et al; CoolCap Study Group. Determinants of outcomes after head cooling for neonatal encephalopathy. Pediatrics 2007; 119 (05) 912-921
    CrossrefPubMedGoogle Scholar
  • 37 Lally PJ, Montaldo P, Oliveira V. , et al; MARBLE Consortium. Magnetic resonance spectroscopy assessment of brain injury after moderate hypothermia in neonatal encephalopathy: a prospective multicentre cohort study. Lancet Neurol 2019; 18 (01) 35-45
    CrossrefPubMedGoogle Scholar
  • 38 Gunn AJ, Wyatt JS, Whitelaw A. , et al; CoolCap Study Group. Therapeutic hypothermia changes the prognostic value of clinical evaluation of neonatal encephalopathy. J Pediatr 2008; 152 (01) 55-58 , 58.e1
    CrossrefPubMedGoogle Scholar
  • 39 Shankaran S, Laptook AR, Tyson JE. , et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Evolution of encephalopathy during whole body hypothermia for neonatal hypoxic-ischemic encephalopathy. J Pediatr 2012; 160 (04) 567-572.e3
    CrossrefPubMedGoogle Scholar
  • 40 Mendler MR, Mendler I, Hassan MA, Mayer B, Bode H, Hummler HD. Predictive value of Thompson-score for long-term neurological and cognitive outcome in term newborns with perinatal asphyxia and hypoxic-ischemic encephalopathy undergoing controlled hypothermia treatment. Neonatology 2018; 114 (04) 341-347
    CrossrefPubMedGoogle Scholar
  • 41 Thorsen P, Jansen-van der Weide MC, Groenendaal F. , et al. The Thompson encephalopathy score and short-term outcomes in asphyxiated newborns treated with therapeutic hypothermia. Pediatr Neurol 2016; 60: 49-53
    CrossrefPubMedGoogle Scholar
  • 42 Horn AR, Swingler GH, Myer L, Linley LL, Chandrasekaran M, Robertson NJ. Early clinical predictors of a severely abnormal amplitude-integrated electroencephalogram at 48 hours in cooled neonates. Acta Paediatr 2013; 102 (08) e378-e384
    CrossrefPubMedGoogle Scholar
  • 43 Giesinger RE, Bailey LJ, Deshpande P, McNamara PJ. Hypoxic-ischemic encephalopathy and therapeutic hypothermia: the hemodynamic perspective. J Pediatr 2017; 180: 22-30.e2
    CrossrefPubMedGoogle Scholar
  • 44 Al Balushi A, Barbosa Vargas S, Maluorni J. , et al. Hypotension and brain injury in asphyxiated newborns treated with hypothermia. Am J Perinatol 2018; 35 (01) 31-38
    Article in Thieme ConnectPubMedGoogle Scholar
  • 45 Mohammad K, Hicks M, Buchhalter J. , et al. Hemodynamic instability associated with increased risk of death or brain injury in neonates with hypoxic ischemic encephalopathy. J Neonatal Perinatal Med 2017; 10 (04) 363-370
    PubMedGoogle Scholar
  • 46 More KS, Sakhuja P, Giesinger RE. , et al. Cardiovascular associations with abnormal brain magnetic resonance imaging in neonates with hypoxic ischemic encephalopathy undergoing therapeutic hypothermia and rewarming. Am J Perinatol 2018; 35 (10) 979-989
    Article in Thieme ConnectPubMedGoogle Scholar
  • 47 Malin GL, Morris RK, Khan KS. Strength of association between umbilical cord pH and perinatal and long term outcomes: systematic review and meta-analysis. BMJ 2010; 340: c1471
    CrossrefPubMedGoogle Scholar
  • 48 Wayock CP, Meserole RL, Saria S. , et al. Perinatal risk factors for severe injury in neonates treated with whole-body hypothermia for encephalopathy. Am J Obstet Gynecol 2014; 211 (01) 41.e1-41.e8
    CrossrefPubMedGoogle Scholar
  • 49 Pappas A, Shankaran S, Laptook AR. , et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Hypocarbia and adverse outcome in neonatal hypoxic-ischemic encephalopathy. J Pediatr 2011; 158 (05) 752-758.e1
    CrossrefPubMedGoogle Scholar
  • 50 Lingappan K, Kaiser JR, Srinivasan C, Gunn AJ. Relationship between PCO2 and unfavorable outcome in infants with moderate-to-severe hypoxic ischemic encephalopathy. Pediatr Res 2016; 80 (02) 204-208
    CrossrefPubMedGoogle Scholar
  • 51 Hansen G, Al Shafouri N, Narvey M, Vallance JK, Srinivasan G. High blood carbon dioxide variability and adverse outcomes in neonatal hypoxic ischemic encephalopathy. J Matern Fetal Neonatal Med 2016; 29 (04) 680-683
    CrossrefPubMedGoogle Scholar
  • 52 Beken S, Aydın B, Dilli D, Erol S, Zenciroğlu A, Okumuş N. Can biochemical markers predict the severity of hypoxic-ischemic encephalopathy?. Turk J Pediatr 2014; 56 (01) 62-68
    PubMedGoogle Scholar
  • 53 Murray DM, Boylan GB, Fitzgerald AP, Ryan CA, Murphy BP, Connolly S. Persistent lactic acidosis in neonatal hypoxic-ischaemic encephalopathy correlates with EEG grade and electrographic seizure burden. Arch Dis Child Fetal Neonatal Ed 2008; 93 (03) F183-F186
    CrossrefPubMedGoogle Scholar
  • 54 Tam EW, Haeusslein LA, Bonifacio SL. , et al. Hypoglycemia is associated with increased risk for brain injury and adverse neurodevelopmental outcome in neonates at risk for encephalopathy. J Pediatr 2012; 161 (01) 88-93
    CrossrefPubMedGoogle Scholar
  • 55 Nadeem M, Murray DM, Boylan GB, Dempsey EM, Ryan CA. Early blood glucose profile and neurodevelopmental outcome at two years in neonatal hypoxic-ischaemic encephalopathy. BMC Pediatr 2011; 11: 10-10
    CrossrefPubMedGoogle Scholar
  • 56 Tan JKG, Minutillo C, McMichael J, Rao S. Impact of hypoglycaemia on neurodevelopmental outcomes in hypoxic ischaemic encephalopathy: a retrospective cohort study. BMJ Paediatr Open 2017; 1 (01) e000175
    PubMedGoogle Scholar
  • 57 Chouthai NS, Sobczak H, Khan R, Subramanian D, Raman S, Rao R. Hyperglycemia is associated with poor outcome in newborn infants undergoing therapeutic hypothermia for hypoxic ischemic encephalopathy. J Neonatal Perinatal Med 2015; 8 (02) 125-131
    CrossrefPubMedGoogle Scholar
  • 58 Basu SK, Kaiser JR, Guffey D, Minard CG, Guillet R, Gunn AJ. ; CoolCap Study Group. Hypoglycaemia and hyperglycaemia are associated with unfavourable outcome in infants with hypoxic ischaemic encephalopathy: a post hoc analysis of the CoolCap Study. Arch Dis Child Fetal Neonatal Ed 2016; 101 (02) F149-F155
    CrossrefPubMedGoogle Scholar
  • 59 Al Shafouri N, Narvey M, Srinivasan G, Vallance J, Hansen G. High glucose variability is associated with poor neurodevelopmental outcomes in neonatal hypoxic ischemic encephalopathy. J Neonatal Perinatal Med 2015; 8 (02) 119-124
    CrossrefPubMedGoogle Scholar
  • 60 Kalteren WS, Ter Horst HJ, den Heijer AE, de Vetten L, Kooi EMW, Bos AF. Perinatal anemia is associated with neonatal and neurodevelopmental outcomes in infants with moderate to severe perinatal asphyxia. Neonatology 2018; 114 (04) 315-322
    CrossrefPubMedGoogle Scholar
  • 61 Zonnenberg IA, Vermeulen RJ, Rohaan MW, van Weissenbruch MM, Groenendaal F, de Vries LS. Severe neonatal anaemia, MRI findings and neurodevelopmental outcome. Neonatology 2016; 109 (04) 282-288
    CrossrefPubMedGoogle Scholar
  • 62 El-Dib M, Chang T, Tsuchida TN, Clancy RR. Amplitude-integrated electroencephalography in neonates. Pediatr Neurol 2009; 41 (05) 315-326
    CrossrefPubMedGoogle Scholar
  • 63 Nash KB, Bonifacio SL, Glass HC. , et al. Video-EEG monitoring in newborns with hypoxic-ischemic encephalopathy treated with hypothermia. Neurology 2011; 76 (06) 556-562
    CrossrefPubMedGoogle Scholar
  • 64 Tsuchida TN. EEG background patterns and prognostication of neonatal encephalopathy in the era of hypothermia. J Clin Neurophysiol 2013; 30 (02) 122-125
    CrossrefPubMedGoogle Scholar
  • 65 Thoresen M, Hellström-Westas L, Liu X, de Vries LS. Effect of hypothermia on amplitude-integrated electroencephalogram in infants with asphyxia. Pediatrics 2010; 126 (01) e131-e139
    CrossrefPubMedGoogle Scholar
  • 66 Sewell EK, Vezina G, Chang T. , et al. Evolution of amplitude-integrated electroencephalogram as a predictor of outcome in term encephalopathic neonates receiving therapeutic hypothermia. Am J Perinatol 2018; 35 (03) 277-285
    Article in Thieme ConnectPubMedGoogle Scholar
  • 67 Massaro AN, Tsuchida T, Kadom N. , et al. aEEG evolution during therapeutic hypothermia and prediction of NICU outcome in encephalopathic neonates. Neonatology 2012; 102 (03) 197-202
    PubMedGoogle Scholar
  • 68 Takenouchi T, Rubens EO, Yap VL, Ross G, Engel M, Perlman JM. Delayed onset of sleep-wake cycling with favorable outcome in hypothermic-treated neonates with encephalopathy. J Pediatr 2011; 159 (02) 232-237
    CrossrefPubMedGoogle Scholar
  • 69 Azzopardi D. Clinical applications of cerebral function monitoring in neonates. Semin Fetal Neonatal Med 2015; 20 (03) 154-163
    CrossrefPubMedGoogle Scholar
  • 70 Briatore E, Ferrari F, Pomero G. , et al. EEG findings in cooled asphyxiated newborns and correlation with site and severity of brain damage. Brain Dev 2013; 35 (05) 420-426
    CrossrefPubMedGoogle Scholar
  • 71 Awal MA, Lai MM, Azemi G, Boashash B, Colditz PB. EEG background features that predict outcome in term neonates with hypoxic ischaemic encephalopathy: A structured review. Clin Neurophysiol 2016; 127 (01) 285-296
    CrossrefPubMedGoogle Scholar
  • 72 De Wispelaere LA, Ouwehand S, Olsthoorn M. , et al. Electroencephalography and brain magnetic resonance imaging in asphyxia comparing cooled and non-cooled infants. Eur J Paediatr Neurol 2019; 23 (01) 181-190
    CrossrefPubMedGoogle Scholar
  • 73 Jain SV, Zempel JM, Srinivasakumar P, Wallendorf M, Mathur A. Early EEG power predicts MRI injury in infants with hypoxic-ischemic encephalopathy. J Perinatol 2017; 37 (05) 541-546
    CrossrefPubMedGoogle Scholar
  • 74 Lynch NE, Stevenson NJ, Livingstone V. , et al. The temporal characteristics of seizures in neonatal hypoxic ischemic encephalopathy treated with hypothermia. Seizure 2015; 33: 60-65
    CrossrefPubMedGoogle Scholar
  • 75 Kharoshankaya L, Stevenson NJ, Livingstone V. , et al. Seizure burden and neurodevelopmental outcome in neonates with hypoxic-ischemic encephalopathy. Dev Med Child Neurol 2016; 58 (12) 1242-1248
    CrossrefPubMedGoogle Scholar
  • 76 Shellhaas RA, Chang T, Tsuchida T. , et al. The American Clinical Neurophysiology Society's guideline on continuous electroencephalography monitoring in neonates. J Clin Neurophysiol 2011; 28 (06) 611-617
    CrossrefPubMedGoogle Scholar
  • 77 Mahfooz N, Weinstock A, Afzal B. , et al. Optimal duration of continuous video-electroencephalography in term infants with hypoxic-ischemic encephalopathy and therapeutic hypothermia. J Child Neurol 2017; 32 (06) 522-527
    CrossrefPubMedGoogle Scholar
  • 78 Braun MH, Bello-Espinosa L, Appendino J, Buchhalter J, Mohammad K, Esser MP. P.060 Utility analysis of continuous video EEG (cvEEG) monitoring during the treatment of hypoxic ischemic encephalopathy (HIE) in the NICU. Can J Neurol Sci 2018; 45 (S2): S31
    PubMedGoogle Scholar
  • 79 Taylor MJ, Murphy WJ, Whyte HE. Prognostic reliability of somatosensory and visual evoked potentials of asphyxiated term infants. Dev Med Child Neurol 1992; 34 (06) 507-515
    PubMedGoogle Scholar
  • 80 Majnemer A, Rosenblatt B. Prediction of outcome at school age in neonatal intensive care unit graduates using neonatal neurologic tools. J Child Neurol 2000; 15 (10) 645-651
    CrossrefPubMedGoogle Scholar
  • 81 Nevalainen P, Lauronen L, Metsäranta M, Lönnqvist T, Ahtola E, Vanhatalo S. Neonatal somatosensory evoked potentials persist during hypothermia. Acta Paediatr 2017; 106 (06) 912-917
    CrossrefPubMedGoogle Scholar
  • 82 Garfinkle J, Sant'Anna GM, Rosenblatt B, Majnemer A, Wintermark P, Shevell MI. Somatosensory evoked potentials in neonates with hypoxic-ischemic encephalopathy treated with hypothermia. Eur J Paediatr Neurol 2015; 19 (04) 423-428
    CrossrefPubMedGoogle Scholar
  • 83 van Laerhoven H, de Haan TR, Offringa M, Post B, van der Lee JH. Prognostic tests in term neonates with hypoxic-ischemic encephalopathy: a systematic review. Pediatrics 2013; 131 (01) 88-98
    CrossrefPubMedGoogle Scholar
  • 84 Cainelli E, Trevisanuto D, Cavallin F, Suppiej A. Evoked potentials predict psychomotor development in neonates with normal MRI after hypothermia for hypoxic-ischemic encephalopathy. Clin Neurophysiol 2018; 129 (06) 1300-1306
    CrossrefPubMedGoogle Scholar
  • 85 Anand NK, Gupta AK, Raj H. Auditory brainstem response in neonates with hypoxic-ischemic-encephalopathy following perinatal asphyxia. Indian Pediatr 1991; 28 (08) 901-907
    PubMedGoogle Scholar
  • 86 Mietzsch U, Parikh NA, Williams AL, Shankaran S, Lasky RE. Effects of hypoxic-ischemic encephalopathy and whole-body hypothermia on neonatal auditory function: a pilot study. Am J Perinatol 2008; 25 (07) 435-441
    Article in Thieme ConnectPubMedGoogle Scholar
  • 87 Liem KD, Greisen G. Monitoring of cerebral haemodynamics in newborn infants. Early Hum Dev 2010; 86 (03) 155-158
    CrossrefPubMedGoogle Scholar
  • 88 Dix LM, van Bel F, Baerts W, Lemmers PM. Comparing near-infrared spectroscopy devices and their sensors for monitoring regional cerebral oxygen saturation in the neonate. Pediatr Res 2013; 74 (05) 557-563
    CrossrefPubMedGoogle Scholar
  • 89 Toet MC, Lemmers PM, van Schelven LJ, van Bel F. Cerebral oxygenation and electrical activity after birth asphyxia: their relation to outcome. Pediatrics 2006; 117 (02) 333-339
    CrossrefPubMedGoogle Scholar
  • 90 Goeral K, Urlesberger B, Giordano V. , et al. Prediction of outcome in neonates with hypoxic-ischemic encephalopathy II: role of amplitude-integrated electroencephalography and cerebral oxygen saturation measured by near-infrared spectroscopy. Neonatology 2017; 112 (03) 193-202
    CrossrefPubMedGoogle Scholar
  • 91 Nakamura S, Koyano K, Jinnai W. , et al. Simultaneous measurement of cerebral hemoglobin oxygen saturation and blood volume in asphyxiated neonates by near-infrared time-resolved spectroscopy. Brain Dev 2015; 37 (10) 925-932
    CrossrefPubMedGoogle Scholar
  • 92 Lemmers PM, Zwanenburg RJ, Benders MJ. , et al. Cerebral oxygenation and brain activity after perinatal asphyxia: does hypothermia change their prognostic value?. Pediatr Res 2013; 74 (02) 180-185
    CrossrefPubMedGoogle Scholar
  • 93 Niezen CK, Bos AF, Sival DA, Meiners LC, Ter Horst HJ. Amplitude-integrated EEG and cerebral near-infrared spectroscopy in cooled, asphyxiated infants. Am J Perinatol 2018; 35 (09) 904-910
    Article in Thieme ConnectPubMedGoogle Scholar
  • 94 Jain SV, Pagano L, Gillam-Krakauer M, Slaughter JC, Pruthi S, Engelhardt B. Cerebral regional oxygen saturation trends in infants with hypoxic-ischemic encephalopathy. Early Hum Dev 2017; 113: 55-61
    CrossrefPubMedGoogle Scholar
  • 95 Billeci L, Marino D, Insana L, Vatti G, Varanini M. Patient-specific seizure prediction based on heart rate variability and recurrence quantification analysis. PLoS One 2018; 13 (09) e0204339
    CrossrefPubMedGoogle Scholar
  • 96 Goulding RM, Stevenson NJ, Murray DM, Livingstone V, Filan PM, Boylan GB. Heart rate variability in hypoxic ischemic encephalopathy: correlation with EEG grade and 2-y neurodevelopmental outcome. Pediatr Res 2015; 77 (05) 681-687
    CrossrefPubMedGoogle Scholar
  • 97 Goulding RM, Stevenson NJ, Murray DM, Livingstone V, Filan PM, Boylan GB. Heart rate variability in hypoxic ischemic encephalopathy during therapeutic hypothermia. Pediatr Res 2017; 81 (04) 609-615
    CrossrefPubMedGoogle Scholar
  • 98 Metzler M, Govindan R, Al-Shargabi T. , et al. Pattern of brain injury and depressed heart rate variability in newborns with hypoxic ischemic encephalopathy. Pediatr Res 2017; 82 (03) 438-443
    CrossrefPubMedGoogle Scholar
  • 99 Massaro AN, Govindan RB, Al-Shargabi T. , et al. Heart rate variability in encephalopathic newborns during and after therapeutic hypothermia. J Perinatol 2014; 34 (11) 836-841
    CrossrefPubMedGoogle Scholar
  • 100 Chau V, Poskitt KJ, Dunham CP, Hendson G, Miller SP. Magnetic resonance imaging in the encephalopathic term newborn. Curr Pediatr Rev 2014; 10 (01) 28-36
    CrossrefPubMedGoogle Scholar
  • 101 Sorokan ST, Jefferies AL, Miller SP. Imaging the term neonatal brain. Paediatr Child Health 2018; 23 (05) 322-328
    CrossrefPubMedGoogle Scholar
  • 102 Groenendaal F, de Vries LS. Fifty years of brain imaging in neonatal encephalopathy following perinatal asphyxia. Pediatr Res 2017; 81 (1-2): 150-155
    CrossrefPubMedGoogle Scholar
  • 103 Natarajan N, Pardo AC. Challenges in neurologic prognostication after neonatal brain injury. Semin Perinatol 2017; 41 (02) 117-123
    CrossrefPubMedGoogle Scholar
  • 104 Barta H, Jermendy A, Kolossvary M. , et al. Prognostic value of early, conventional proton magnetic resonance spectroscopy in cooled asphyxiated infants. BMC Pediatr 2018; 18 (01) 302
    CrossrefPubMedGoogle Scholar
  • 105 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; 78 (18) 1420-1427
    CrossrefPubMedGoogle Scholar
  • 106 Heinz ER, Provenzale JM. Imaging findings in neonatal hypoxia: a practical review. AJR Am J Roentgenol 2009; 192 (01) 41-47
    CrossrefPubMedGoogle Scholar
  • 107 Rutherford M, Biarge MM, Allsop J, Counsell S, Cowan F. MRI of perinatal brain injury. Pediatr Radiol 2010; 40 (06) 819-833
    CrossrefPubMedGoogle Scholar
  • 108 Barkovich AJ, Miller SP, Bartha A. , et al. MR imaging, MR spectroscopy, and diffusion tensor imaging of sequential studies in neonates with encephalopathy. AJNR Am J Neuroradiol 2006; 27 (03) 533-547
    PubMedGoogle Scholar
  • 109 Cheong JLY, Coleman L, Hunt RW. , et al; Infant Cooling Evaluation Collaboration. Prognostic utility of magnetic resonance imaging in neonatal hypoxic-ischemic encephalopathy: substudy of a randomized trial. Arch Pediatr Adolesc Med 2012; 166 (07) 634-640
    PubMedGoogle Scholar
  • 110 Rutherford M, Ramenghi LA, Edwards AD. , et al. Assessment of brain tissue injury after moderate hypothermia in neonates with hypoxic-ischaemic encephalopathy: a nested substudy of a randomised controlled trial. Lancet Neurol 2010; 9 (01) 39-45
    CrossrefPubMedGoogle Scholar
  • 111 Shankaran S, Barnes PD, Hintz SR. , et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Brain injury following trial of hypothermia for neonatal hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 2012; 97 (06) F398-F404
    PubMedGoogle Scholar
  • 112 Sánchez Fernández I, Morales-Quezada JL, Law S, Kim P. Prognostic value of brain magnetic resonance imaging in neonatal hypoxic-ischemic encephalopathy: a meta-analysis. J Child Neurol 2017; 32 (13) 1065-1073
    CrossrefPubMedGoogle Scholar
  • 113 Thayyil S, Chandrasekaran M, Taylor A. , et al. Cerebral magnetic resonance biomarkers in neonatal encephalopathy: a meta-analysis. Pediatrics 2010; 125 (02) e382-e395
    CrossrefPubMedGoogle Scholar
  • 114 Barkovich AJ, Hajnal BL, Vigneron D. , et al. Prediction of neuromotor outcome in perinatal asphyxia: evaluation of MR scoring systems. AJNR Am J Neuroradiol 1998; 19 (01) 143-149
    PubMedGoogle Scholar
  • 115 Miller SP, Ramaswamy V, Michelson D. , et al. Patterns of brain injury in term neonatal encephalopathy. J Pediatr 2005; 146 (04) 453-460
    CrossrefPubMedGoogle Scholar
  • 116 Xu Q, Chau V, Sanguansermsri C. , et al. Pattern of brain injury predicts long-term epilepsy following neonatal encephalopathy. J Child Neurol 2019 Doi: 10.1177/0883073818822361. [Epub ahead of print]
    PubMedGoogle Scholar
  • 117 de Vries LS, Jongmans MJ. Long-term outcome after neonatal hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed 2010; 95 (03) F220-F224
    CrossrefPubMedGoogle Scholar
  • 118 Steinman KJ, Gorno-Tempini ML, Glidden DV. , et al. Neonatal watershed brain injury on magnetic resonance imaging correlates with verbal IQ at 4 years. Pediatrics 2009; 123 (03) 1025-1030
    CrossrefPubMedGoogle Scholar
  • 119 Rutherford MA, Pennock JM, Counsell SJ. , et al. Abnormal magnetic resonance signal in the internal capsule predicts poor neurodevelopmental outcome in infants with hypoxic-ischemic encephalopathy. Pediatrics 1998; 102 (2, Pt 1): 323-328
    CrossrefPubMedGoogle Scholar
  • 120 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
    CrossrefPubMedGoogle Scholar
  • 121 Rollins N, Booth T, Morriss MC, Sanchez P, Heyne R, Chalak L. Predictive value of neonatal MRI showing no or minor degrees of brain injury after hypothermia. Pediatr Neurol 2014; 50 (05) 447-451
    CrossrefPubMedGoogle Scholar
  • 122 Wong DS, Poskitt KJ, Chau V. , et al. Brain injury patterns in hypoglycemia in neonatal encephalopathy. AJNR Am J Neuroradiol 2013; 34 (07) 1456-1461
    CrossrefPubMedGoogle Scholar
  • 123 Salas J, Tekes A, Hwang M, Northington FJ, Huisman TAGM. 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 (03) 185-197
    CrossrefPubMedGoogle Scholar
  • 124 Skranes JH, Elstad M, Thoresen M, Cowan FM, Stiris T, Fugelseth D. Hypothermia makes cerebral resistance index a poor prognostic tool in encephalopathic newborns. Neonatology 2014; 106 (01) 17-23
    CrossrefPubMedGoogle Scholar
  • 125 Twomey E, Twomey A, Ryan S, Murphy J, Donoghue VB. MR imaging of term infants with hypoxic-ischaemic encephalopathy as a predictor of neurodevelopmental outcome and late MRI appearances. Pediatr Radiol 2010; 40 (09) 1526-1535
    CrossrefPubMedGoogle Scholar
  • 126 Sarnat HB, Sarnat MS. Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study. Arch Neurol 1976; 33 (10) 696-705
    CrossrefPubMedGoogle Scholar
  • 127 Thompson CM, Puterman AS, Linley LL. , et al. The value of a scoring system for hypoxic ischaemic encephalopathy in predicting neurodevelopmental outcome. Acta Paediatr 1997; 86 (07) 757-761
    CrossrefPubMedGoogle Scholar
  • 128 Chandrasekaran M, Chaban B, Montaldo P, Thayyil S. Predictive value of amplitude-integrated EEG (aEEG) after rescue hypothermic neuroprotection for hypoxic ischemic encephalopathy: a meta-analysis. J Perinatol 2017; 37 (06) 684-689
    CrossrefPubMedGoogle Scholar
  • 129 Del Río R, Ochoa C, Alarcon A, Arnáez J, Blanco D, García-Alix A. Amplitude integrated electroencephalogram as a prognostic tool in neonates with hypoxic-ischemic encephalopathy: a systematic review. PLoS One 2016; 11 (11) e0165744
    CrossrefPubMedGoogle Scholar
  • 130 Osredkar D, Toet MC, van Rooij LG, van Huffelen AC, Groenendaal F, de Vries LS. Sleep-wake cycling on amplitude-integrated electroencephalography in term newborns with hypoxic-ischemic encephalopathy. Pediatrics 2005; 115 (02) 327-332
    CrossrefPubMedGoogle Scholar
  • 131 Takenouchi T, Rubens EO, Yap VL, Ross G, Engel M, Perlman JM. Delayed onset of sleep-wake cycling with favorable outcome in hypothermic-treated neonates with encephalopathy. J Pediatr 2011; 159 (02) 232-237
    CrossrefPubMedGoogle Scholar
  • 132 Dunne JM, Wertheim D, Clarke P. , et al. Automated electroencephalographic discontinuity in cooled newborns predicts cerebral MRI and neurodevelopmental outcome. Arch Dis Child Fetal Neonatal Ed 2017; 102 (01) F58-F64
    CrossrefPubMedGoogle Scholar
  • 133 Fitzgerald MP, Massey SL, Fung FW, Kessler SK, Abend NS. High electroencephalographic seizure exposure is associated with unfavorable outcomes in neonates with hypoxic-ischemic encephalopathy. Seizure 2018; 61: 221-226
    CrossrefPubMedGoogle Scholar