Am J Perinatol 2023; 40(05): 475-488
DOI: 10.1055/s-0041-1731278
Review Article

Cerebral Blood Flow of the Neonatal Brain after Hypoxic–Ischemic Injury

1   Department of Radiology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
,
Sandra Saade-Lemus*
1   Department of Radiology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
2   Department of Neurology, Brigham and Women's Hospital & Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
,
Colbey Freeman
1   Department of Radiology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
3   Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania
,
Matthew Kirschen
4   Department of Anesthesiology and Critical Care Medicine, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
,
Hao Huang
1   Department of Radiology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
3   Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania
,
Arastoo Vossough
1   Department of Radiology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
3   Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania
,
1   Department of Radiology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
3   Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania
› Author Affiliations
Funding None.

Abstract

Objective Hypoxic–ischemic encephalopathy (HIE) in infants can have long-term adverse neurodevelopmental effects and markedly reduce quality of life. Both the initial hypoperfusion and the subsequent rapid reperfusion can cause deleterious effects in brain tissue. Cerebral blood flow (CBF) assessment in newborns with HIE can help detect abnormalities in brain perfusion to guide therapy and prognosticate patient outcomes.

Study Design The review will provide an overview of the pathophysiological implications of CBF derangements in neonatal HIE, current and emerging techniques for CBF quantification, and the potential to utilize CBF as a physiologic target in managing neonates with acute HIE.

Conclusion The alterations of CBF in infants during hypoxia-ischemia have been studied by using different neuroimaging techniques, including nitrous oxide and xenon clearance, transcranial Doppler ultrasonography, contrast-enhanced ultrasound, arterial spin labeling MRI, 18F-FDG positron emission tomography, near-infrared spectroscopy (NIRS), functional NIRS, and diffuse correlation spectroscopy. Consensus is lacking regarding the clinical significance of CBF estimations detected by these different modalities. Heterogeneity in the imaging modality used, regional versus global estimations of CBF, time for the scan, and variables impacting brain perfusion and cohort clinical characteristics should be considered when translating the findings described in the literature to routine practice and implementation of therapeutic interventions.

Key Points

  • Hypoxic–ischemic injury in infants can result in adverse long-term neurologic sequelae.

  • Cerebral blood flow is a useful biomarker in neonatal hypoxic–ischemic injury.

  • Imaging modality, variables affecting cerebral blood flow, and patient characteristics affect cerebral blood flow assessment.

* These authors contributed equally to this study.




Publication History

Received: 28 November 2020

Accepted: 12 May 2021

Article published online:
05 July 2021

© 2021. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Levene MI, Sands C, Grindulis H, Moore JR. Comparison of two methods of predicting outcome in perinatal asphyxia. Lancet 1986; 1 (8472): 67-69
  • 2 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
  • 3 Kurinczuk JJ, White-Koning M, Badawi N. Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum Dev 2010; 86 (06) 329-338
  • 4 Douglas-Escobar M, Weiss MD. Hypoxic-ischemic encephalopathy: a review for the clinician. JAMA Pediatr 2015; 169 (04) 397-403
  • 5 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
  • 6 Harriman T, Bradshaw WT, Blake SM. The use of whole body cooling in the treatment of hypoxic-ischemic encephalopathy. Neonatal Netw 2017; 36 (05) 273-279
  • 7 Shepherd E, Salam RA, Middleton P, Han S, Makrides M, McIntyre S. et al. Neonatal interventions for preventing cerebral palsy: an overview of Cochrane Systematic Reviews. Cochrane Database Syst Rev 2018; 20 (06) CD012409
  • 8 Martinello K, Hart AR, Yap S, Mitra S, Robertson NJ. Management and investigation of neonatal encephalopathy: 2017 update. Arch Dis Child Fetal Neonatal Ed 2017; 102 (04) F346-F358
  • 9 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
  • 10 Fantini S, Sassaroli A, Tgavalekos KT, Kornbluth J. Cerebral blood flow and autoregulation: current measurement techniques and prospects for noninvasive optical methods. Neurophotonics 2016; 3 (03) 031411
  • 11 Panerai RB, Kelsall AW, Rennie JM, Evans DH. Cerebral autoregulation dynamics in premature newborns. Stroke 1995; 26 (01) 74-80
  • 12 Gunn AJ, Bennet L. Fetal hypoxia insults and patterns of brain injury: insights from animal models. Clin Perinatol 2009; 36 (03) 579-593
  • 13 Volpe JJ, Herscovitch P, Perlman JM, Kreusser KL, Raichle ME. Positron emission tomography in the asphyxiated term newborn: parasagittal impairment of cerebral blood flow. Ann Neurol 1985; 17 (03) 287-296
  • 14 Pryds O, Edwards AD. Cerebral blood flow in the newborn infant. Arch Dis Child Fetal Neonatal Ed 1996; 74 (01) F63-F69
  • 15 Narayanan S, Schmithorst V, Panigrahy A. Arterial spin labeling in pediatric neuroimaging. Semin Pediatr Neurol 2020; 33: 100799
  • 16 Meek JH, Tyszczuk L, Elwell CE, Wyatt JS. Cerebral blood flow increases over the first three days of life in extremely preterm neonates. Arch Dis Child Fetal Neonatal Ed 1998; 78 (01) F33-F37
  • 17 Chiron C, Raynaud C, Mazière B. et al. Changes in regional cerebral blood flow during brain maturation in children and adolescents. J Nucl Med 1992; 33 (05) 696-703
  • 18 Epstein HT. Stages of increased cerebral blood flow accompany stages of rapid brain growth. Brain Dev 1999; 21 (08) 535-539
  • 19 Wintermark M, Lepori D, Cotting J. et al. Brain perfusion in children: evolution with age assessed by quantitative perfusion computed tomography. Pediatrics 2004; 113 (06) 1642-1652
  • 20 Takahashi T, Shirane R, Sato S, Yoshimoto T. Developmental changes of cerebral blood flow and oxygen metabolism in children. AJNR Am J Neuroradiol 1999; 20 (05) 917-922
  • 21 Kehrer M, Goelz R, Krägeloh-Mann I, Schöning M. Measurement of volume of cerebral blood flow in healthy preterm and term neonates with ultrasound. Lancet 2002; 360 (9347): 1749-1750
  • 22 Iwata S, Tachtsidis I, Takashima S, Matsuishi T, Robertson NJ, Iwata O. Dual role of cerebral blood flow in regional brain temperature control in the healthy newborn infant. Int J Dev Neurosci 2014; 37: 1-7
  • 23 Kusaka T, Okubo K, Nagano K, Isobe K, Itoh S. Cerebral distribution of cardiac output in newborn infants. Arch Dis Child Fetal Neonatal Ed 2005; 90 (01) F77-F78
  • 24 Ouyang M, Liu P, Jeon T. et al. Heterogeneous increases of regional cerebral blood flow during preterm brain development: Preliminary assessment with pseudo-continuous arterial spin labeled perfusion MRI. Neuroimage 2017; 147 (147) 233-242
  • 25 Altman DI, Powers WJ, Perlman JM, Herscovitch P, Volpe SL, Volpe JJ. Cerebral blood flow requirement for brain viability in newborn infants is lower than in adults. Ann Neurol 1988; 24 (02) 218-226
  • 26 Pryds O, Greisen G. Preservation of single-flash visual evoked potentials at very low cerebral oxygen delivery in preterm infants. Pediatr Neurol 1990; 6 (03) 151-158
  • 27 Vutskits L. Cerebral blood flow in the neonate. Paediatr Anaesth 2014; 24 (01) 22-29
  • 28 Todd MM, Weeks J. Comparative effects of propofol, pentobarbital, and isoflurane on cerebral blood flow and blood volume. J Neurosurg Anesthesiol 1996; 8 (04) 296-303
  • 29 Harreld JH, Helton KJ, Kaddoum RN. et al. The effects of propofol on cerebral perfusion MRI in children. Neuroradiology 2013; 55 (08) 1049-1056
  • 30 Milan A, Freato F, Vanzo V, Chiandetti L, Zaramella P. Influence of ventilation mode on neonatal cerebral blood flow and volume. Early Hum Dev 2009; 85 (07) 415-419
  • 31 Bell AH, Miller SL, Castillo-Melendez M, Malhotra A. The neurovascular unit: effects of brain insults during the perinatal period. Front Neurosci 2020; 13: 1452
  • 32 Abbott NJ, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006; 7 (01) 41-53
  • 33 Bano S, Chaudhary V, Garga UC. Neonatal hypoxic-ischemic encephalopathy: a radiological review. J Pediatr Neurosci 2017; 12 (01) 1-6
  • 34 Lin L, Wang X, Yu Z. Ischemia-reperfusion injury in the brain: mechanisms and potential therapeutic strategies, Biochem Pharmacol. 2016 5. 04
  • 35 McKinney AM, Teksam M, Felice R. et al. Diffusion-weighted imaging in the setting of diffuse cortical laminar necrosis and hypoxic-ischemic encephalopathy. AJNR Am J Neuroradiol 2004; 25 (10) 1659-1665
  • 36 Cohan SL, Mun SK, Petite J, Correia J, Tavelra Da Silva AT, Waldhorn RE. Cerebral blood flow in humans following resuscitation from cardiac arrest. Stroke 1989; 20 (06) 761-765
  • 37 Hanigan WC, Aldag J, Sabo RA, Rose J, Aaland M. Strangulation injuries in children. Part 2. Cerebrovascular hemodynamics. J Trauma 1996; 40 (01) 73-77
  • 38 Wijdicks EF, Campeau NG, Miller GM. MR imaging in comatose survivors of cardiac resuscitation. AJNR Am J Neuroradiol 2001; 22 (08) 1561-1565
  • 39 Cabaj A, Bekiesińska-Figatowska M, Mądzik J. MRI patterns of hypoxic-ischemic brain injury in preterm and full term infants - classical and less common MR findings. Pol J Radiol 2012; 77 (03) 71-76
  • 40 Liauw L, Palm-Meinders IH, van der Grond J. et al. Differentiating normal myelination from hypoxic-ischemic encephalopathy on T1-weighted MR Images: a new approach. AJNR Am J Neuroradiol 2007; 28 (04) 660-665
  • 41 Ilves P, Lintrop M, Talvik I, Muug K, Asser K, Veinla M. Developmental changes in cerebral and visceral blood flow velocity in healthy neonates and infants. J Ultrasound Med 2008; 27 (02) 199-207
  • 42 Meric P, Seylaz J, Correze JL, Luft A, Mamo H. Measurement of regional cerebral blood flow by intravenous injection of Xe133. Med Prog Technol 1979; 6 (02) 53-63
  • 43 Frewen TC, Kissoon N, Kronick J. et al. Cerebral blood flow, cross-brain oxygen extraction, and fontanelle pressure after hypoxic-ischemic injury in newborn infants. J Pediatr 1991; 118 (02) 265-271
  • 44 Ashwal S, Schneider S, Thompson J. Xenon computed tomography measuring cerebral blood flow in the determination of brain death in children. Ann Neurol 1989; 25 (06) 539-546
  • 45 Wintermark M, Sesay M, Barbier E. et al. Comparative overview of brain perfusion imaging techniques. Stroke 2005; 36 (09) e83-e99
  • 46 LaRovere KL, O'Brien NF. Transcranial Doppler sonography in pediatric neurocritical care: a review of clinical applications and case illustrations in the pediatric intensive care unit. J Ultrasound Med 2015; 34 (12) 2121-2132
  • 47 Bulas DI. Transcranial Doppler: applications in neonates and children. Ultrasound Clin 2009; 4 (04) 533-551
  • 48 Iordanova B, Li L, Clark RSB, Manole MD. Alterations in cerebral blood flow after resuscitation from cardiac arrest. Front Pediatr 2017; 5: 174
  • 49 Alvarez-Fernández JA, Pérez-Quintero R. Use of transcranial Doppler ultrasound in the management of post-cardiac arrest syndrome. Resuscitation 2009; 80 (11) 1321-1322
  • 50 Forster DE, Koumoundouros E, Saxton V, Fedai G, Holberton J. Cerebral blood flow velocities and cerebrovascular resistance in normal-term neonates in the first 72  hours. J Paediatr Child Health 2018; 54 (01) 61-68
  • 51 Liu J, Cao H-Y, Huang X-H, Wang Q. The pattern and early diagnostic value of Doppler ultrasound for neonatal hypoxic-ischemic encephalopathy. J Trop Pediatr 2007; 53 (05) 351-354
  • 52 Stark JE, Seibert JJ. Cerebral artery Doppler ultrasonography for prediction of outcome after perinatal asphyxia. J Ultrasound Med 1994; 13 (08) 595-600
  • 53 Archer LNJ, Levene MI, Evans DH. Cerebral artery Doppler ultrasonography for prediction of outcome after perinatal asphyxia. Lancet 1986; 2 (8516): 1116-1118
  • 54 Gray PH, Tudehope DI, Masel JP. et al. Perinatal hypoxic-ischaemic brain injury: prediction of outcome. Dev Med Child Neurol 1993; 35 (11) 965-973
  • 55 Blankenberg FG, Loh NN, Norbash AM. et al. Impaired cerebrovascular autoregulation after hypoxic-ischemic injury in extremely low-birth-weight neonates: detection with power and pulsed wave Doppler US. Radiology 1997; 205 (02) 563-568
  • 56 Hwang M, De Jong Jr RM, Herman S. et al. Novel contrast-enhanced ultrasound evaluation in neonatal hypoxic ischemic injury: clinical application and future directions. J Ultrasound Med 2017; 36 (11) 2379-2386
  • 57 Hwang M. Introduction to contrast-enhanced ultrasound of the brain in neonates and infants: current understanding and future potential. Pediatr Radiol 2019; 49 (02) 254-262
  • 58 Dietrich CF, Averkiou M, Nielsen MB. et al. How to perform contrast-enhanced ultrasound (CEUS). Ultrasound Int Open 2018; 4 (01) E2-E15
  • 59 Hwang M, Sridharan A, Darge K. et al. Novel quantitative contrast-enhanced ultrasound detection of hypoxic ischemic injury in neonates and infants: pilot study 1. J Ultrasound Med 2019; 38 (08) 2025-2038
  • 60 Hwang M, Back SJ, Didier RA. et al. Pediatric contrast-enhanced ultrasound: optimization of techniques and dosing. Pediatr Radiol 2021; 51: 2147-2160
  • 61 Wintermark P, Hansen A, Gregas MC. et al. Brain perfusion in asphyxiated newborns treated with therapeutic hypothermia. AJNR Am J Neuroradiol 2011; 32 (11) 2023-2029
  • 62 Christophe C, Fonteyne C, Ziereisen F. et al. Value of MR imaging of the brain in children with hypoxic coma. AJNR Am J Neuroradiol 2002; 23 (04) 716-723
  • 63 Biagi L, Abbruzzese A, Bianchi MC, Alsop DC, Del Guerra A, Tosetti M. Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling. J Magn Reson Imaging 2007; 25 (04) 696-702
  • 64 Huisman TAGM, Sorensen AG. Perfusion-weighted magnetic resonance imaging of the brain: techniques and application in children. Eur Radiol 2004; 14 (01) 59-72
  • 65 Miranda MJ, Olofsson K, Sidaros K. Noninvasive measurements of regional cerebral perfusion in preterm and term neonates by magnetic resonance arterial spin labeling. Pediatr Res 2006; 60 (03) 359-363
  • 66 Wang J, Licht DJ. Pediatric perfusion MR imaging using arterial spin labeling. Neuroimaging Clin N Am 2006; 16 (01) 149-167 , ix ix.
  • 67 Wang J, Licht DJ, Silvestre DW, Detre JA. Why perfusion in neonates with congenital heart defects is negative--technical issues related to pulsed arterial spin labeling. Magn Reson Imaging 2006; 24 (03) 249-254
  • 68 Rana L, Sood D, Chauhan R. et al. MR imaging of hypoxic ischemic encephalopathy - distribution patterns and ADC value correlations. Eur J Radiol Open 2018; 5: 215-220
  • 69 Wintermark P, Moessinger AC, Gudinchet F, Meuli R. Temporal evolution of MR perfusion in neonatal hypoxic-ischemic encephalopathy. J Magn Reson Imaging 2008; 27 (06) 1229-1234
  • 70 De Vis JB, Hendrikse J, Petersen ET. et al. Arterial spin-labelling perfusion MRI and outcome in neonates with hypoxic-ischemic encephalopathy. Eur Radiol 2015; 25 (01) 113-121
  • 71 Proisy M, Corouge I, Legouhy A. et al. Changes in brain perfusion in successive arterial spin labeling MRI scans in neonates with hypoxic-ischemic encephalopathy. Neuroimage Clin 2019; 24: 101939
  • 72 Zheng Q, Martin-Saavedra JS, Saade-Lemus S. et al. Cerebral pulsed arterial spin labeling perfusion weighted imaging predicts language and motor outcomes in neonatal hypoxic-ischemic encephalopathy. Front Pediatr 2020; 8: 576489
  • 73 Zheng Q, Viaene AN, Freeman CW, Hwang M. Radiologic-pathologic evidence of brain injury: hypoperfusion in the Papez circuit results in poor neurodevelopmental outcomes in neonatal hypoxic ischemic encephalopathy. Childs Nerv Syst ChNS Off J Int Soc Pediatr Neurosurg. 2020; DOI: 10.1007/s00381-020-04795-0.
  • 74 Detre JA, Leigh JS, Williams DS, Koretsky AP. Perfusion imaging. Magn Reson Med 1992; 23 (01) 37-45
  • 75 Williams DS, Detre JA, Leigh JS, Koretsky AP. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci USA 1992; 89 (01) 212-216
  • 76 De Vis JB, Petersen ET, Alderliesten T. et al. Non-invasive MRI measurements of venous oxygenation, oxygen extraction fraction and oxygen consumption in neonates. Neuroimage 2014; 95: 185-192
  • 77 Ferré J-C, Bannier E, Raoult H, Mineur G, Carsin-Nicol B, Gauvrit J-Y. Arterial spin labeling (ASL) perfusion: techniques and clinical use. Diagn Interv Imaging 2013; 94 (12) 1211-1223
  • 78 Boudes E, Gilbert G, Leppert IR. et al. Measurement of brain perfusion in newborns: pulsed arterial spin labeling (PASL) versus pseudo-continuous arterial spin labeling (pCASL). Neuroimage Clin 2014; 6: 126-133
  • 79 Alsop DC, Detre JA, Golay X. et al. Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 2015; 73 (01) 102-116
  • 80 Liu P, Qi Y, Lin Z, Guo Q, Wang X, Lu H. Assessment of cerebral blood flow in neonates and infants: a phase-contrast MRI study. Neuroimage 2019; 185 (185) 926-933
  • 81 Tang S, Liu X, He L, Liu B, Qin B, Feng C. Application of a 3D pseudocontinuous arterial spin-labeled perfusion MRI scan combined with a postlabeling delay value in the diagnosis of neonatal hypoxic-ischemic encephalopathy. PLoS One 2019; 14 (07) e0219284
  • 82 McGuirt D. Alternatives to sedation and general anesthesia in pediatric magnetic resonance imaging: a literature review. Radiol Technol 2016; 88 (01) 18-26
  • 83 Gao Y, Goodnough CL, Erokwu BO. et al. Arterial spin labeling-fast imaging with steady-state free precession (ASL-FISP): a rapid and quantitative perfusion technique for high-field MRI. NMR Biomed 2014; 27 (08) 996-1004
  • 84 Bandres J, Yao L, Nemoto EM, Yonas H, Darby J. Effects of dobutamine and dopamine on whole brain blood flow and metabolism in unanesthetized monkeys. J Neurosurg Anesthesiol 1992; 4 (04) 250-256
  • 85 de Nadal M, Munar F, Poca MA, Sahuquillo J, Garnacho A, Rosselló J. Cerebral hemodynamic effects of morphine and fentanyl in patients with severe head injury: absence of correlation to cerebral autoregulation. Anesthesiology 2000; 92 (01) 11-19
  • 86 Basu S, Hess S, Nielsen Braad P-E, Olsen BB, Inglev S, Høilund-Carlsen PF. The basic principles of FDG-PET/CT imaging. PET Clin 2014; 9 (04) 355-370 , v
  • 87 Proisy M, Mitra S, Uria-Avellana C. et al. Brain perfusion imaging in neonates: an overview. AJNR Am J Neuroradiol 2016; 37 (10) 1766-1773
  • 88 Berger A. How does it work? Positron emission tomography. BMJ 2003; 326 (7404): 1449
  • 89 Huisman MC, van Golen LW, Hoetjes NJ. et al. Cerebral blood flow and glucose metabolism in healthy volunteers measured using a high-resolution PET scanner. EJNMMI Res 2012; 2 (01) 63
  • 90 Frackowiak RS, Lenzi GL, Jones T, Heather JD. Quantitative measurement of regional cerebral blood flow and oxygen metabolism in man using 15O and positron emission tomography: theory, procedure, and normal values. J Comput Assist Tomogr 1980; 4 (06) 727-736
  • 91 Wang Z, Mascarenhas C, Jia X. Positron emission tomography after ischemic brain injury: current challenges and future developments. Transl Stroke Res 2020; 11 (04) 628-642
  • 92 Azzarelli B, Caldemeyer KS, Phillips JP, DeMyer WE. Hypoxic-ischemic encephalopathy in areas of primary myelination: a neuroimaging and PET study. Pediatr Neurol 1996; 14 (02) 108-116
  • 93 Shi Y, Zhao J-N, Liu L. et al. Changes of positron emission tomography in newborn infants at different gestational ages, and neonatal hypoxic-ischemic encephalopathy. Pediatr Neurol 2012; 46 (02) 116-123
  • 94 Thorngren-Jerneck K, Ohlsson T, Sandell A. et al. Cerebral glucose metabolism measured by positron emission tomography in term newborn infants with hypoxic ischemic encephalopathy. Pediatr Res 2001; 49 (04) 495-501
  • 95 Rudolph AM. Cerebral glucose deficiency versus oxygen deficiency in neonatal encephalopathy. J Neonatal Perinatal Med 2018; 11 (02) 115-120
  • 96 Shetty AN, Lucke AM, Liu P. et al. Cerebral oxygen metabolism during and after therapeutic hypothermia in neonatal hypoxic-ischemic encephalopathy: a feasibility study using magnetic resonance imaging. Pediatr Radiol 2019; 49 (02) 224-233
  • 97 Doyle LW, Nahmias C, Firnau G, Kenyon DB, Garnett ES, Sinclair JC. Regional cerebral glucose metabolism of newborn infants measured by positron emission tomography. Dev Med Child Neurol 1983; 25 (02) 143-151
  • 98 Koc ZP, Balci TA, Akarsu S, Unal K. The role of positron emission tomography/CT in hypoxic ischaemic encephalopathy in children. BMJ Case Rep 2013; 2013 (Jan): 2
  • 99 Volpe JJ, Herscovitch P, Perlman JM, Raichle ME. Positron emission tomography in the newborn: extensive impairment of regional cerebral blood flow with intraventricular hemorrhage and hemorrhagic intracerebral involvement. Pediatrics 1983; 72 (05) 589-601
  • 100 Altman DI, Perlman JM, Volpe JJ, Powers WJ. Cerebral oxygen metabolism in newborns. Pediatrics 1993; 92 (01) 99-104
  • 101 Toet MC, Lemmers PMA. Brain monitoring in neonates. Early Hum Dev 2009; 85 (02) 77-84
  • 102 Rhee CJ, da Costa CS, Austin T, Brady KM, Czosnyka M, Lee JK. Neonatal cerebrovascular autoregulation. Pediatr Res 2018; 84 (05) 602-610
  • 103 Fantini S, Sassaroli A. Frequency-domain techniques for cerebral and functional near-infrared spectroscopy. Front Neurosci 2020; 14: 300
  • 104 Edwards AD, Wyatt JS, Richardson C, Delpy DT, Cope M, Reynolds EO. Cotside measurement of cerebral blood flow in ill newborn infants by near infrared spectroscopy. Lancet 1988; 2 (8614): 770-771
  • 105 Toet MC, Lemmers PMA, van Schelven LJ, van Bel F. Cerebral oxygenation and electrical activity after birth asphyxia: their relation to outcome. Pediatrics 2006; 117 (02) 333-339
  • 106 Ancora G, Maranella E, Grandi S. et al. Early predictors of short term neurodevelopmental outcome in asphyxiated cooled infants. A combined brain amplitude integrated electroencephalography and near infrared spectroscopy study. Brain Dev 2013; 35 (01) 26-31
  • 107 Lemmers PMA, Zwanenburg RJ, Benders MJNL. et al. Cerebral oxygenation and brain activity after perinatal asphyxia: does hypothermia change their prognostic value?. Pediatr Res 2013; 74 (02) 180-185
  • 108 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
  • 109 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
  • 110 Al-Rawi PG, Kirkpatrick PJ. Tissue oxygen index: thresholds for cerebral ischemia using near-infrared spectroscopy. Stroke 2006; 37 (11) 2720-2725
  • 111 Hyttel-Sorensen S, Pellicer A, Alderliesten T. et al. Cerebral near infrared spectroscopy oximetry in extremely preterm infants: phase II randomised clinical trial. BMJ 2015; 350: g7635
  • 112 Tsuji M, Saul JP, du Plessis A. et al. Cerebral intravascular oxygenation correlates with mean arterial pressure in critically ill premature infants. Pediatrics 2000; 106 (04) 625-632
  • 113 Brady K, Joshi B, Zweifel C. et al. Real-time continuous monitoring of cerebral blood flow autoregulation using near-infrared spectroscopy in patients undergoing cardiopulmonary bypass. Stroke 2010; 41 (09) 1951-1956
  • 114 Plomgaard AM, Alderliesten T, van Bel F, Benders M, Claris O, Cordeiro M. et al. No neurodevelopmental benefit of cerebral oximetry in the first randomised trial (SafeBoosC II) in preterm infants during the first days of life. Acta Paediatr Oslo Nor 1992 2019; 108 (02) 275-81
  • 115 Toet MC, Flinterman A, Laar Iv. et al. Cerebral oxygen saturation and electrical brain activity before, during, and up to 36  hours after arterial switch procedure in neonates without pre-existing brain damage: its relationship to neurodevelopmental outcome. Exp Brain Res 2005; 165 (03) 343-350
  • 116 Wintermark P, Hansen A, Warfield SK, Dukhovny D, Soul JS. Near-infrared spectroscopy versus magnetic resonance imaging to study brain perfusion in newborns with hypoxic-ischemic encephalopathy treated with hypothermia. Neuroimage 2014; 85 (Pt 1): 287-293
  • 117 Dix LML, van Bel F, Baerts W, Lemmers PMA. Comparing near-infrared spectroscopy devices and their sensors for monitoring regional cerebral oxygen saturation in the neonate. Pediatr Res 2013; 74 (05) 557-563
  • 118 Mitra S, Bale G, Meek J, Tachtsidis I, Robertson NJ. Cerebral near infrared spectroscopy monitoring in term infants with hypoxic ischemic encephalopathy-a systematic review. Front Neurol 2020; 11: 393
  • 119 Lloyd-Fox S, Blasi A, Elwell CE. Illuminating the developing brain: the past, present and future of functional near infrared spectroscopy. Neurosci Biobehav Rev 2010; 34 (03) 269-284
  • 120 Quaresima V, Bisconti S, Ferrari M. A brief review on the use of functional near-infrared spectroscopy (fNIRS) for language imaging studies in human newborns and adults. Brain Lang 2012; 121 (02) 79-89
  • 121 Peng C, Hou X. Applications of functional near-infrared spectroscopy (fNIRS) in neonates. Neurosci Res. [Internet]. [cited 2021 Feb 25]. Accessed December 30, 2020 from: https://www.sciencedirect.com/science/article/pii/S016801022030482X
  • 122 de Roever I, Bale G, Mitra S, Meek J, Robertson NJ, Tachtsidis I. Investigation of the pattern of the hemodynamic response as measured by functional near-infrared spectroscopy (fNIRS) studies in newborns, less than a month old: a systematic review. Front Hum Neurosci 2018; 12: 371
  • 123 Peña M, Maki A, Kovacić D. et al. Sounds and silence: an optical topography study of language recognition at birth. Proc Natl Acad Sci U S A 2003; 100 (20) 11702-11705
  • 124 Grossmann T, Oberecker R, Koch SP, Friederici AD. The developmental origins of voice processing in the human brain. Neuron 2010; 65 (06) 852-858
  • 125 Chen S, Sakatani K, Lichty W, Ning P, Zhao S, Zuo H. Auditory-evoked cerebral oxygenation changes in hypoxic-ischemic encephalopathy of newborn infants monitored by near infrared spectroscopy. Early Hum Dev 2002; 67 (1-2): 113-121
  • 126 Chiarelli AM, Zappasodi F, Di Pompeo F, Merla A. Simultaneous functional near-infrared spectroscopy and electroencephalography for monitoring of human brain activity and oxygenation: a review. Neurophotonics 2017; 4 (04) 041411
  • 127 Buckley EM, Parthasarathy AB, Grant PE, Yodh AG, Franceschini MA. Diffuse correlation spectroscopy for measurement of cerebral blood flow: future prospects. Neurophotonics 2014; 1 (01) 011009
  • 128 Farzam P, Buckley EM, Lin P-Y. et al. Shedding light on the neonatal brain: probing cerebral hemodynamics by diffuse optical spectroscopic methods. Sci Rep 2017; 7 (01) 15786
  • 129 Giovannella M, Contini D, Pagliazzi M. et al. BabyLux device: a diffuse optical system integrating diffuse correlation spectroscopy and time-resolved near-infrared spectroscopy for the neuromonitoring of the premature newborn brain. Neurophotonics 2019; 6 (02) 025007
  • 130 Buckley EM, Patel SD, Miller BF, Franceschini MA, Vannucci SJ. In vivo monitoring of cerebral hemodynamics in the immature rat: effects of hypoxia-ischemia and hypothermia. Dev Neurosci 2015; 37 (4-5): 407-416
  • 131 Dehaes M, Aggarwal A, Lin P-Y. et al. Cerebral oxygen metabolism in neonatal hypoxic ischemic encephalopathy during and after therapeutic hypothermia. J Cereb Blood Flow Metab 2014; 34 (01) 87-94
  • 132 Armstead WM. Cerebral blood flow autoregulation and dysautoregulation. Anesthesiol Clin 2016; 34 (03) 465-477
  • 133 Massaro AN, Govindan RB, Vezina G. et al. Impaired cerebral autoregulation and brain injury in newborns with hypoxic-ischemic encephalopathy treated with hypothermia. J Neurophysiol 2015; 114 (02) 818-824
  • 134 Lee JK, Poretti A, Perin J. et al. Optimizing cerebral autoregulation may decrease neonatal regional hypoxic-ischemic brain injury. Dev Neurosci 2017; 39 (1-4): 248-256
  • 135 Carrasco M, Perin J, Jennings JM. et al. Cerebral autoregulation and conventional and diffusion tensor imaging magnetic resonance imaging in neonatal hypoxic-ischemic encephalopathy. Pediatr Neurol 2018; 82: 36-43
  • 136 Massaro AN, Bouyssi-Kobar M, Chang T, Vezina LG, du Plessis AJ, Limperopoulos C. Brain perfusion in encephalopathic newborns after therapeutic hypothermia. AJNR Am J Neuroradiol 2013; 34 (08) 1649-1655
  • 137 Howlett JA, Northington FJ, Gilmore MM. et al. Cerebrovascular autoregulation and neurologic injury in neonatal hypoxic-ischemic encephalopathy. Pediatr Res 2013; 74 (05) 525-535
  • 138 Greisen G. Cerebral blood flow and oxygenation in infants after birth asphyxia. Clinically useful information?. Early Hum Dev 2014; 90 (10) 703-705