Preconditioning and postinsult therapies for perinatal hypoxic-ischemic injury at term

Anesthesiology

Volumn 113, Issue 1, 2010, Pages 233-249

  Sanders, Robert D ^a   Manning, Helen J ^b   Robertson, Nicola J ^c   Ma, Daqing ^d   Edwards, A David ^e   Hagberg, Henrik ^f   Maze, Mervyn ^g,h  

^a Intensive Care and Pain Medicine   (United Kingdom)

^b Intensive Care and Pain Medicine ^*  (United Kingdom)

^c MEDICAL RESEARCH COUNCIL   (United Kingdom)

^d QUEEN CHARLOTTE S AND CHELSEA HOSPITAL   (United Kingdom)

^e JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^f UNIVERSITY COLLEGE HOSPITAL   (United Kingdom)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

^h San Francisco State Unversity   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ALLOPURINOL; ANTIINFLAMMATORY AGENT; BARBITURIC ACID DERIVATIVE; BENZODIAZEPINE DERIVATIVE; BUMETANIDE; CALCIUM CHANNEL BLOCKING AGENT; CLONIDINE; DEXAMETHASONE; DEXMEDETOMIDINE; DIAZEPAM; ERYTHROPOIETIN; ISOFLURANE; KETAMINE; MANNITOL; MELATONIN; MIDAZOLAM; MINOCYCLINE; NEUROPROTECTIVE AGENT; NITROUS OXIDE; OPIATE; PENTOBARBITAL; PHENOBARBITAL; PHENYTOIN; S 100BETA; SEVOFLURANE; THIOPENTAL; TOPIRAMATE; UNCLASSIFIED DRUG; XANTHINE OXIDASE INHIBITOR; XENON; ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT; ANTICONVULSIVE AGENT; ANTIOXIDANT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTOXIN; SCAVENGER;

APOPTOSIS; BENIGN CHILDHOOD EPILEPSY; BRAIN BLOOD FLOW; BRAIN DISEASE; BRAIN INJURY; BRAIN PERFUSION; CEREBRAL PALSY; CLINICAL TRIAL; DRUG MEGADOSE; EXCITOTOXICITY; HUMAN; HYPEROXIA; HYPOCAPNIA; ISCHEMIC PRECONDITIONING; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PERINATAL CARE; PERINATAL HYPOXIC ISCHEMIC ENCEPHALOPATHY; PRIORITY JOURNAL; RESUSCITATION; REVIEW; SIDE EFFECT; STROKE; ANIMAL; BRAIN ISCHEMIA; DRUG ANTAGONISM; FEMALE; INFLAMMATION; METHODOLOGY; PREGNANCY; PRENATAL DIAGNOSIS; SEIZURE;

ADRENERGIC ALPHA-AGONISTS; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTICONVULSANTS; ANTIOXIDANTS; APOPTOSIS; ERYTHROPOIETIN; FEMALE; FREE RADICAL SCAVENGERS; HUMANS; HYPEROXIA; HYPOCAPNIA; HYPOXIA-ISCHEMIA, BRAIN; INFLAMMATION; ISCHEMIC PRECONDITIONING; NEUROPROTECTIVE AGENTS; NEUROTOXINS; PREGNANCY; PRENATAL DIAGNOSIS; RECEPTORS, N-METHYL-D-ASPARTATE; SEIZURES;

EID: 77954177555     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e3181dc1b84     Document Type: Review

References (163)

1. Shankaran S, Laptook AR: Hypothermia as a treatment for birth asphyxia. Clin Obstet Gynecol 2007; 50:624-635
2. Whitelaw A, Thoresen M: Clinical trials of treatments after perinatal asphyxia. Curr Opin Pediatr 2002; 14: 664-668
3. Gonzalez FF, Ferriero DM: Therapeutics for neonatal brain injury. Pharmacol Ther 2008; 120:43-53
4. Lawn JE, Cousens S, Zupan J; Lancet neonatal survival steering team: Four million neonatal deaths: When? Where? Why? Lancet 2005; 365:891-900
5. Rennie JM, Hagmann CF, Robertson NJ: Outcome after intrapartum hypoxic ischemia at term. Semin Fetal Neonatal Med 2007; 12:398-407
6. Odd DE, Lewis G, Whitelaw A, Gunnell D: Resuscitation at birth and cognition at 8 years of age: A cohort study. Lancet 2009; 373:1615-1622
7. Rennie JM, Hagmann CF, Robertson NJ: The baby who was depressed at birth, Neonatal Cerebral Investigation Text Book. Edited by Hagmann CF, Robertson NJ, Rennie JM. Cambridge, Cambridge University Press, 2008, pp 130-172
8. Azzopardi D, Wyatt JS, Cady EB, Delpy DT, Baudin J, Stewart AL, Hope PL, Hamilton PA, Reynolds EO: Prognosis of newborn infants with hypoxic-ischemic brain injury assessed by phosphorus magnetic resonance spec-troscopy. Pediatr Res 1989; 25:445-451
9. Lorek A, Takei Y, Cady EB, Wyatt JS, Penrice J, Edwards AD, Peebles D, Wylezinska M, Owen-Reece H, Kirkbride V, Cooper CE, Aldridge RF, Roth SC, Brown G, Delpy DT, Reynolds EO: Delayed (secondary) cerebral energy failure after acute hypoxia-ischemia in the newborn piglet: Continuous 48-hour studies by phosphorus magnetic resonance spectroscopy. Pediatr Res 1994; 36:699-706 (Pubitemid 24357779)
10. Hagberg H, Thornberg E, Blennow M, Kjellmer I, Lager-crantz H, Thiringer K, Hamberger A, Sandberg M: Excitatory amino acids in the cerebrospinal fluid of asphyxiated infants: Relationship to hypoxic-ischemic encephalopa-thy. Acta Paediatr 1993; 82:925-929
11. Haberny KA, Paule MG, Scallet AC, Sistare FD, Lester DS, Hanig JP, Slikker W Jr: Ontogeny of the N-methyl-D-aspar-tate (NMDA) receptor system and susceptibility to neu-rotoxicity. Toxicol Sci 2002; 68:9-17
12. Ikonomidou C, Mosinger JL, Salles KS, Labruyere J, Olney JW: Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-methyl-aspar-tate neurotoxicity. J Neurosci 1989; 9:2809-2818
13. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH: Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994; 12:529-540
14. Blomgren K, Hagberg H: Free radicals, mitochondria, and hypoxia-ischemia in the developing brain. Free Radic Biol Med 2006; 40:388-397
15. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K: The K\+/Clco-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999; 397:251-255
16. Puka-Sundvall M, Gajkowska B, Cholewinski M, Blomgren K, Lazarewicz JW, Hagberg H: Subcellular distribution of calcium and ultrastructural changes after cerebral hy-poxia-ischemia in immature rats. Brain Res Dev Brain Res 2000; 125:31-41
17. Gilland E, Puka-Sundvall M, Hillered L, Hagberg H: Mito-chondrial function and energy metabolism after hypoxia-ischemia in the immature rat brain: Involvement of NMDA-receptors. J Cereb Blood Flow Metab 1998; 18: 297-304
18. Kutzsche S, Ilves P, Kirkeby OJ, Saugstad OD: Hydrogen peroxide production in leukocytes during cerebral hyp-oxia and reoxygenation with 100% or 21% oxygen in newborn piglets. Pediatr Res 2001; 49:834-842
19. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y, Hagberg H, Blomgren K: The influence of age on apopto-tic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 2005; 12:162-176
20. Edwards AD, Mehmet H: Apoptosis in perinatal hypoxic-ischemic cerebral damage. Neuropathol Appl Neurobiol 1996; 22:494-498
21. Wang X, Carlsson Y, Basso E, Zhu C, Rousset CI, Rasola A, Johansson BR, Blomgren K, Mallard C, Bernardi P, Forte MA, Hagberg H: Developmental shift of cyclophilin D contribution to hypoxic-ischemic brain injury. J Neurosci 2009; 29:2588-2596
22. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vöckler J, Dikranian K, Tenkova TI, Stefovska V, Turski L, Olney JW: Blockade of NMDA receptors and apoptotic neurodegen-eration in the developing brain. Science 1999; 283:70-74
23. Bittigau P, Sifringer M, Genz K, Reith E, Pospischil D, Govindarajalu S, Dzietko M, Pesditschek S, Mai I, Dikra-nian K, Olney JW, Ikonomidou C: Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc Natl Acad Sci USA 2002; 99:15089-15094 (Pubitemid 35334614)
24. Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorumski CF, Olney JW, Wozniak DF: Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci 2003; 23:876-882
25. Sanders RD, Ma D, Brooks P, Maze M: Balancing paediat-ric anaesthesia: Preclinical insights into analgesia, hypnosis, neuroprotection, and neurotoxicity. Br J Anaesth 2008; 101:597-609
26. Ma D, Hossain M, Chow A, Arshad M, Battson RM, Sanders RD, Mehmet H, Edwards AD, Franks NP, Maze M: Xenon and hypothermia combine to provide neuropro-tection from neonatal asphyxia. Ann Neurol 2005; 58: 182-193
27. Liu Y, Barks JD, Xu G, Silverstein FS: Topiramate extends the therapeutic window for hypothermia-mediated neu-roprotection after stroke in neonatal rats. Stroke 2004; 35:1460-1465
28. Grether JK, Nelson KB: Maternal infection and cerebral palsy in infants of normal birth weight. JAMA 1997; 27:207-211
29. Aziz K, Chadwick M, Baker M, Andrews W: Ante-and intra-partum factors that predict increased need for neonatal resuscitation. Resuscitation 2008; 79:444-452
30. Badawi N, Kurinczuk JJ, Keogh JM, Alessandri LM, O'Sullivan F, Burton PR, Pemberton PJ, Stanley FJ: Intra-partum risk factors for newborn encephalopathy: The Western Australian case-control study. BMJ 1998; 317: 1554-1558 (Pubitemid 28550235)
31. Lieberman E, Eichenwald E, Mathur G, Richardson D, Heffner L, Cohen A: Intrapartum fever and unexplained seizures in term infants. Pediatrics 2000; 106:983-988
32. Edwards AD, Tan S: Perinatal infections, prematurity and brain injury. Curr Opin Pediatr 2006; 18:119-124
33. Yoon BH, Jun JK, Romero R, Park KH, Gomez R, Choi JH, Kim IO: Amniotic fluid inflammatory cytokines (interleu-kin-6, interleukin-1beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 1997; 177:19-26
34. Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, Hagberg H: Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 2001; 13:1101-1106
35. Loddick SA, Turnbull AV, Rothwell NJ: Cerebral interleu-kin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 1998; 18:176-179
36. Iwata O, Iwata S, Thornton JS, De Vita E, Bainbridge A, Herbert L, Scaravilli F, Peebles D, Wyatt JS, Cady EB, Robertson NJ: Therapeutic time window duration decreases with increasing severity of cerebral hypoxia-isch-emia under normothermia and delayed hypothermia in the newborn piglet. Brain Res 2007; 1154:173-180
37. Roth SC, Baudin J, Cady E, Johal K, Townsend JP, Wyatt JS, Reynolds EO, Stewart A: Relation of deranged neonatal cerebral oxidative metabolism with neurodevelopmental outcome and head circumference at 4 years. Dev Med Child Neurol 1997; 39:718-725
38. Robertson NJ, Cowan FM, Cox IJ, Edwards AD: Brain alkaline intracellular pH after neonatal encephalopathy. Ann Neurol 2002; 52:732-742
39. McGowan JE, Perlman JM: Glucose management during and after intensive delivery room resuscitation. Clin Peri-natol 2006; 33:183-189
40. Lou HC, Lassen NA, Friis-Hansen B: Impaired autoregula-tion of cerebral blood flow in the distressed newborn infant. J Pediatr 1979; 94:118-121
41. Volpe J: Hypoxic-ischemic encephalopathy: Biochemical and Physiological Aspects, Neurology of The Newborn, 5th edition. Edited by Volpe J. Philadelphia, Elsevier, 2008, pp 247-325
42. Badawi N, Kurinczuk JJ, Keogh JM, Alessandri LM, O'Sullivan F, Burton PR, Pemberton PJ, Stanley FJ: Ante-partum risk factors for newborn encephalopathy: The Western Australian case-control study. BMJ 1998; 317: 1549-1553 (Pubitemid 28550234)
43. Cowan F, Rutherford M, Groenendaal F, Eken P, Mercuri E, Bydder GM, Meiners LC, Dubowitz LM, de Vries LS: Origin and timing of brain lesions in term infants with neonatal encephalopathy. Lancet 2003; 361:736-742
44. American Academy of Pediatrics, American College of Obstetricians and Gynecologists: Neonatal encephalopa-thy and cerebral palsy: Defining the pathogenesis and pathophysiology. Washington, DC, American Academy of Pediatrics, 2003
45. Graham EM, Petersen SM, Christo DK, Fox HE: Intrapar-tum electronic fetal heart rate monitoring and the prevention of perinatal brain injury. Obstet Gynecol 2006; 108:656-666
46. Kubli FW, Hon EH, Khazin AF, Takemura H: Observations on heart rate and pH in the human fetus during labor. Am J Obstet Gynecol 1969; 104:1190-1206
47. Nelson KB, Dambrosia JM, Ting TY, Grether JK: Uncertain value of electronic fetal monitoring in predicting cerebral palsy. N Engl J Med 1996; 334:613-618
48. Low JA, Victory R, Derrick EJ: Predictive value of electronic fetal monitoring for intrapartum fetal asphyxia with metabolic acidosis. Obstet Gynecol 1999; 93:285-291
49. Ikeda T, Murata Y, Quilligan EJ, Choi BH, Parer JT, Doi S, Park SD: Physiologic and histologic changes in near-term fetal lambs exposed to asphyxia by partial umbilical cord occlusion. Am J Obstet Gynecol 1998; 178:24-32 (Pubitemid 28302789)
50. Alfirevic Z, Devane D, Gyte GM: Continuous cardiotocog-raphy (CTG) as a form of electronic fetal monitoring (EFM) for fetal assessment during labor. Cochrane Database Syst Rev 2006; 3:CD006066
51. Vintzileos AM, Antsaklis A, Varvarigos I, Papas C, Sofatzis I, Montgomery JT: A randomized trial of intrapartum electronic fetal heart rate monitoring versus intermittent auscultation. Obstet Gynecol 1993; 81:899-907
52. Wiberg-Itzel E, Lipponer C, Norman M, Herbst A, Prebensen D, Hansson A, Bryngelsson AL, Christoffersson M, Sennström M, Wennerholm UB, Nordström L: Determination of pH or lactate in fetal scalp blood in management of intrapartum fetal distress: Randomized controlled multicentre trial. BMJ 2008; 336:1284-1287
53. ACOG Committee on Obstetric Practice: ACOG Committee Opinion No. 348, November 2006: Umbilical cord blood gas and acid-base analysis. Obstet Gynecol 2006; 108:1319-1322
54. Graham EM, Ruis KA, Hartman AL, Northington FJ, Fox HE: A systematic review of the role of intrapartum hy-poxia-ischemia in the causation of neonatal encephalop-athy. Am J Obstet Gynecol 2008; 199:587-595
55. Neilson JP: Fetal electrocardiogram (ECG) for fetal monitoring during labour. Cochrane Database Syst Rev 2006; 3:CD000116
56. Siristatidis C, Salamalekis E, Kassanos D, Loghis C, Creat-sas G: Evaluation of fetal intrapartum hypoxia by middle, cerebral and umbilical artery Doppler velocimetry with simultaneous cardiotocography and pulse oximetry, Arch Gynecol Obstet, 2004, 270,265-270
57. American Academy of Pediatrics and American College of Obstetricians and Genecologists: Care of the Neonate, Guidelines for Perinatal Care, 5th edition. Edited by Gil-strap LC, Oh W. Elk Grove Village, IL, American Academy of Pediatrics, 2002, pp 187-235
58. Casey BM, McIntire DD, Leveno KJ: The continuing value of the Apgar score for the assessment of newborn infants. N Engl J Med 2001; 344:467-471
59. Sarnat HB, Sarnat MS: Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study. Arch Neurol 1976; 33:696-705
60. Shah DK, de Vries LS, Hellström-Westas L, Toet MC, Inder TE: Amplitude-integrated electroencephalography in the newborn: A valuable tool. Pediatrics 2008; 122:863-865
61. Gluckman PD, Wyatt JS, Azzopardi D, Ballard R, Edwards AD, Ferriero DM, Polin RA, Robertson CM, Thoresen M, Whitelaw A, Gunn A: Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: Multicentre randomized trial. Lancet 2005; 365:663-670
62. Azzopardi DV, Strohm B, Edwards AD, Dyet L, Halliday HL, Juszczak E, Kapellou O, Levene M, Marlow N, Porter E, Thoresen M, Whitelaw A, Brocklehurst P: Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med 2009; 361:1349-1358
63. 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: 333-339
64. Cady EB, Iwata O, Bainbridge A, Wyatt JS, Robertson NJ: Phosphorus magnetic resonance spectroscopy 2 h after perinatal cerebral hypoxia-ischemia prognosticates outcome in the newborn piglet. J Neurochem 2008; 107: 1027-1035
65. Hanrahan JD, Sargentoni J, Azzopardi D, Manji K, Cowan FM, Rutherford MA, Cox IJ, Bell JD, Bryant DJ, Edwards AD: Cerebral metabolism within 18 hours of birth asphyxia: A proton magnetic resonance spectroscopy study. Pediatr Res 1996; 39:584-590
66. Gustavsson M, Anderson MF, Mallard C, Hagberg H: Hy-poxic preconditioning confers long-term reduction of brain injury and improvement of neurological ability in immature rats. Pediatr Res 2005; 57:305-309
67. Cai Z, Fratkin JD, Rhodes PG: Prenatal ischemia reduces neuronal injury caused by neonatal hypoxia-ischemia in rats. Neuroreport 1997; 8:1393-1398
68. Gustavsson M, Mallard C, Vannucci SJ, Wilson MA, Johnston MV, Hagberg H: Vascular response to hypoxic preconditioning in the immature brain. J Cereb Blood Flow Metab 2007; 27:928-938 (Pubitemid 46659031)
69. Gustavsson M, Wilson MA, Mallard C, Rousset C, Johnston MV, Hagberg H: Global gene expression in the developing rat brain after hypoxic preconditioning: Involvement of apoptotic mechanisms? Pediatr Res 2007; 61:444-450
70. Brucklacher RM, Vannucci RC, Vannucci SJ: Hypoxic preconditioning increases brain glycogen and delays energy depletion from hypoxia-ischemia in the immature rat. Dev Neurosci 2002; 24:411-417
71. Hamrick SE, McQuillen PS, Jiang X, Mu D, Madan A, Ferriero DM: A role for hypoxia-inducible factor-1alpha in desferoxamine neuroprotection. Neurosci Lett 2005; 379:96-100
72. Ma D, Hossain M, Pettet GK, Luo Y, Lim T, Akimov S, Sanders RD, Franks NP, Maze M: Xenon preconditioning reduces brain damage from neonatal asphyxia in rats. J Cereb Blood Flow Metab 2006; 26:199-208
73. Ma D, Lim T, Xu J, Tang H, Wan Y, Zhao H, Hossain M, Maxwell PH, Maze M: Xenon preconditioning protects against renal ischemic-reperfusion injury via HIF-1alpha activation. J Am Soc Nephrol 2009; 20:713-720
74. Li QF, Zhu YS, Jiang H: Isoflurane preconditioning activates HIF-1alpha, iNOS and Erk1/2 and protects against oxygen-glucose deprivation neuronal injury. Brain Res 2008; 1245:26-35
75. Bantel C, Maze M, Trapp S: Neuronal preconditioning by inhalational anesthetics: Evidence for the role of plas-malemmal adenosine triphosphate-sensitive potassium channels. ANESTHESIOLOGY 2009; 110:986-995
76. Miao B, Yin XH, Pei DS, Zhang QG, Zhang GY: Neuro-protective effects of preconditioning ischemia on isch-emic brain injury through down-regulating activation of JNK1/2 via N-methyl-D-aspartate receptor-mediated Akt1 activation. J Biol Chem 2005; 280:21693-21699 (Pubitemid 40827815)
77. Zhao P, Zuo Z: Isoflurane preconditioning induces neu-roprotection that is inducible nitric oxide synthase-de-pendent in neonatal rats. ANESTHESIOLOGY 2004; 101:695-703
78. Luo Y, Ma D, Ieong E, Sanders RD, Yu B, Hossain M, Maze M: Xenon and sevoflurane protect against brain injury in a neonatal asphyxia model. ANESTHESIOLOGY 2008; 109: 782-789
79. Yeo ST, Holdcroft A, Yentis SM, Stewart A, Bassett P: Analgesia with sevoflurane during labour: II. Sevoflurane compared with Entonox for labour analgesia. Br J An-aesth 2007; 98:110-115 (Pubitemid 44896760)
80. Rouse DJ, Hirtz DG, Thom E, Varner MW, Spong CY, Mercer BM, Iams JD, Wapner RJ, Sorokin Y, Alexander JM, Harper M, Thorp JM Jr, Ramin SM, Malone FD, Carpenter M, Miodovnik M, Moawad A, O'Sullivan MJ, Peace-man AM, Hankins GD, Langer O, Caritis SN, Roberts JM: A randomized, controlled trial of magnesium sulfate for the prevention of cerebral palsy. N Engl J Med 2008; 359:895-905
81. Doyle LW, Crowther CA, Middleton P, Marret S, Rouse D: Magnesium sulphate for women at risk of preterm birth for neuroprotection of the fetus. Cochrane Database Syst Rev 2009:CD004661
82. Greenwood K, Cox P, Mehmet H, Penrice J, Amess PN, Cady EB, Wyatt JS, Edwards AD: Magnesium sulfate treatment after transient hypoxia-ischemia in the newborn piglet does not protect against cerebral damage. Pediatr Res 2000; 48:346-350
83. Groenendaal F, Rademaker CM, Toet MC, de Vries LS: Effects of magnesium sulphate on amplitude-integrated continuous EEG in asphyxiated term neonates. Acta Pae-diatr 2002; 91:1073-1077
84. Dribben WH, Creeley CE, Wang HH, Smith DJ, Farber NB, Olney JW: High dose magnesium sulfate exposure induces apoptotic cell death in the developing neonatal mouse brain. Neonatology 2009; 96:23-32
85. Eicher DJ, Wagner CL, Katikaneni LP, Hulsey TC, Bass WT, Kaufman DA, Horgan MJ, Languani S, Bhatia JJ, Givelichian LM, Sankaran K, Yager JY: Moderate hypothermia in neonatal encephalopathy: Efficacy outcomes. Pediatr Neurol 2005; 32:11-17 (Pubitemid 40018099)
86. Shankaran S, Laptook AR, Ehrenkranz RA, Tyson JE, McDonald SA, Donovan EF, Fanaroff AA, Poole WK, Wright LL, Higgins RD, Finer NN, Carlo WA, Duara S, Oh W, Cotten CM, Stevenson DK, Stoll BJ, Lemons JA, Guillet R, Jobe AH; National Institute of Child Health and Human Development Neonatal Research Network: Whole-body hypothermia for neonates with hypoxic-ischemic en-cephalopathy. N Engl J Med 2005; 353:1574-1584
87. Westin B, Miller JA, Nyberg R, Wedenberg E: Neonatal asphyxia pallida treated with hypothermia alone or with hypothermia and transfusion of oxygenated blood. Surgery 1959; 45:868-879
88. Cordey R: Hypothermia in resuscitating newborns in white asphyxia: A report of 14 cases. Obstet Gynecol 1964; 24:760-767
89. Silverman WA, Fertig JW, Berger AP: The influence of the thermal environment upon the survival of newly born premature infants. Pediatrics 1958; 22:876-886
90. Busto R, Dietrich WD, Globus MY, Ginsberg MD: Post-ischemic moderate hypothermia inhibits CA1 hippocam-pal ischemic neuronal injury. Neurosci Lett 1989; 101: 299-304
91. Thoresen M, Penrice J, Lorek A, Cady EB, Wylezinska M, Kirkbride V, Cooper CE, Brown GC, Edwards AD, Wyatt JS, Reynolds EO: Mild hypothermia after severe transient hy-poxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr Res 1995; 37:667-670
92. Jacobs S, Hunt R, Tarnow-Mordi W, Inder T, Davis P: Cooling for newborns with hypoxic ischaemic encepha-lopathy. Cochrane Database Syst Rev 2007:CD003311
93. 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; 98:631-635
94. Rutherford MA, Azzopardi D, Whitelaw A, Cowan F, Re-nowden S, Edwards AD, Thoresen M: Mild hypothermia and the distribution of cerebral lesions in neonates with hypoxic-ischemic encephalopathy. Pediatrics 2005; 16: 1001-1006
95. Rutherford M, Ramenghi LA, Edwards AD, Brocklehurst P, Halliday H, Levene M, Strohm B, Thoresen M, Whitelaw A, Azzopardi D: Assessment of brain tissue injury after moderate hypothermia in neonates with hy-poxic-ischaemic encephalopathy: A nested substudy of a randomised controlled trial. Lancet Neurol 2010; 9:39-45
96. Thoresen M, Satas S, Puka-Sundvall M, Whitelaw A, Hall-ström A, Løberg EM, Ungerstedt U, Steen PA, Hagberg H: Post-hypoxic hypothermia reduces cerebrocortical release of NO and excitotoxins. Neuroreport 1997; 8:3359-3362
97. Zeevalk GD, Nicklas WJ: Hypothermia, metabolic stress, and NMDA-mediated excitotoxicity. J Neurochem 1993; 61:1445-1453
98. Kil HY, Zhang J, Piantadosi CA: Brain temperature alters hydroxyl radical production during cerebral ischemia/reperfusion in rats. J Cereb Blood Flow Metab 1996; 16:100-106
99. Iwata O, Thornton JS, Sellwood MW, Iwata S, Sakata Y, Noone MA, O'Brien FE, Bainbridge A, De Vita E, Raivich G, Peebles D, Scaravilli F, Cady EB, Ordidge R, Wyatt JS, Robertson NJ: Depth of delayed cooling alters neuropro-tection pattern after hypoxia-ischemia. Ann Neurol 2005; 58:75-87
100. Thoresen M, Satas S, Loberg EM, Whitelaw A, Acolet D, Lindgren C, Penrice J, Robertson N, Haug E, Steen P: Twenty-four hours of mild hypothermia in unsedated newborn pigs starting after a severe global hypoxic-isch-emic insult is not neuroprotective. Pediatr Res 2001; 50:405-411
101. Westermaier T, Zausinger S, Baethmann A, Steiger HJ, Schmid-Elsaesser R: No additional neuroprotection provided by barbiturate-induced burst suppression under mild hypothermic conditions in rats subjected to reversible focal ischemia. J Neurosurg 2000; 93:835-844
102. Jatana M, Singh I, Singh AK, Jenkins D: Combination of systemic hypothermia and N-acetylcysteine attenuates hypoxic-ischemic brain injury in neonatal rats. Pediatr Res 2006; 59:684-689
103. Levene M: Minimising neonatal brain injury: How research in the past five years has changed my clinical practice. Arch Dis Child 2007; 92:261-265
104. Fritz KI, Ashraf QM, Mishra OP, Delivoria-Papadopoulos M: Effect of moderate hypocapnic ventilation on nuclear DNA fragmentation and energy metabolism in the cerebral cortex of newborn piglets, Pediatr Res, 2001, 50, 586-589
105. Victor S, Appleton RE, Beirne M, Marson AG, Weindling AM: Effect of carbon dioxide on background cerebral electrical activity and fractional oxygen extraction in very low birth weight infants just after birth. Pediatr Res 2005; 58:579-585
106. Vannucci RC, Brucklacher RM, Vannucci SJ: Effect of carbon dioxide on cerebral metabolism during hypoxia-ischemia in the immature rat. Pediatr Res 1997; 42:24-29
107. Robertson NJ, Bhakoo K, Puri BK, Edwards AD, Cox IJ: Hypothermia and amiloride preserve energetics in a neonatal brain slice model. Pediatr Res 2005; 58:288-296
108. Kofke WA, Garman RH, Garman R, Rose ME: Opioid neurotoxicity: Fentanyl-induced exacerbation of cerebral ischemia in rats. Brain Res 1999; 818:326-334
109. Clark WM, Raps EC, Tong DC, Kelly RE; The Cervene Stroke Study Investigators: Cervene (Nalmefene) in acute ischemic stroke: Final results of a phase III efficacy study. Stroke 2000; 31:1234-1239
110. Anand KJ, Barton BA, McIntosh N, Lagercrantz H, Pelausa E, Young TE, Vasa R: Analgesia and sedation in preterm neonates who require ventilatory support: Results from the NOPAIN trial. Neonatal Outcome and Prolonged Analgesia in Neonates. Arch Pediatr Adolesc Med 1999; 153:331-338
111. Mujsce DJ, Towfighi J, Stern D, Vannucci RC: Mannitol therapy in perinatal hypoxic-ischemic brain damage in rats. Stroke 1990; 21:1210-1214 (Pubitemid 20255419)
112. Levene MI, Evans D: Medical management of raised intra-cranial pressure after severe birth asphyxia. Arch Dis Child 1985; 60:12-16
113. Wirrell EC, Armstrong EA, Osman LD, Yager JY: Prolonged seizures exacerbate perinatal hypoxic-ischemic brain damage. Pediatr Res 2001; 50:445-454
114. Miller SP, Weiss J, Barnwell A, Ferriero DM, Latal-Hajnal B, Ferrer-Rogers A, Newton N, Partridge JC, Glidden DV, Vign-eron DB, Barkovich AJ: Seizure-associated brain injury in term newborns with perinatal asphyxia. Neurology 2002; 58:542-548
115. Glass HC, Glidden D, Jeremy RJ, Barkovich AJ, Ferriero DM, Miller SP: Clinical neonatal seizures are independently associated with outcome in infants at risk for hypoxic-ischemic brain injury. J Pediatr 2009; 155:318-323
116. Hall RT, Hall FK, Daily DK: High-dose phenobarbital therapy in term newborn infants with severe perinatal asphyxia: A randomized, prospective study with three-year follow-up. J Pediatr 1998; 132:345-348
117. Goldberg RN, Moscoso P, Bauer CR, Bloom FL, Curless RG, Burke B, Bancalari E: Use of barbiturate therapy in severe perinatal asphyxia: A randomized controlled trial. J Pediatr 1986; 109:851-856
118. Ruth V, Virkola K, Paetau R, Raivio KO: Early high-dose phenobarbital treatment for prevention of hypoxic-isch-emic brain damage in very low birth weight infants. J Pediatr 1988; 112:81-86
119. Follett PL, Deng W, Dai W, Talos DM, Massillon LJ, Rosenberg PA, Volpe JJ, Jensen FE: Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leu-komalacia: A protective role for topiramate. J Neurosci 2004; 24:4412-4420
120. Glier C, Dzietko M, Bittigau P, Jarosz B, Korobowicz E, Ikonomidou C: Therapeutic doses of topiramate are not toxic to the developing rat brain. Exp Neurol 2004; 187:403-409
121. Schubert S, Brandl U, Brodhun M, Ulrich C, Spaltmann J, Fiedler N, Bauer R: Neuroprotective effects of topiramate after hypoxia-ischemia in newborn piglets. Brain Res 2005; 1058:129-223
122. Silverstein FS, Jensen FE, Inder T, Hellstrom-Westas L, Hirtz D, Ferriero DM: Improving the treatment of neonatal seizures: National Institute of Neurological Disorders and Stroke workshop report. J Pediatr 2008; 153:12-15
123. 2-adrenoceptor agonists on perinatal excitotoxic brain injury: Comparison of clonidine and dexmedetomidine. ANESTHESIOLOGY 2002; 96:134-141
124. Dean JM, George S, Naylor AS, Mallard C, Gunn AJ, Bennet L: Partial neuroprotection with low-dose infusion of the alpha2-adrenergic receptor agonist clonidine after severe hypoxia in preterm fetal sheep. Neuropharmacology 2008; 55:166-174
125. 2A-adrenoceptor subtype. Eur J Pharmacol 2004; 502:87-97
126. Rajakumaraswamy N, Ma D, Hossain M, Sanders RD, Franks NP, Maze M: Neuroprotective interaction produced by xenon and dexmedetomidine on in vitro and in vivo neuronal injury models. Neurosci Lett 2006; 409: 128-133
127. Guerguerian AM, Brambrink AM, Traystman RJ, Huganir RL, Martin LJ: Altered expression and phosphorylation of N-methyl-D-aspartate receptors in piglet striatum after hypoxia-ischemia. Brain Res Mol Brain Res 2002; 104: 66-80
128. Robinson S, Li Q, Dechant A, Cohen ML: Neonatal loss of gamma-aminobutyric acid pathway expression after human perinatal brain injury. J Neurosurg 2006; 104:396-408
129. Puka-Sundvall M, Hallin U, Zhu C, Wang X, Karlsson JO, Blomgren K, Hagberg H: NMDA blockade attenuates caspase-3 activation and DNA fragmentation after neonatal hypoxia-ischemia. Neuroreport 2000; 11:2833-2836
130. Ikonomidou C, Mosinger JL, OlneyJW: Hypothermia enhances protective effect of MK-801 against hypoxic/ischemic brain damage in infant rats. Brain Res 1989; 487: 184-187
131. Alkan T, Kahveci N, Buyukuysal L, Korfali E, Ozluk K: Neuroprotective effects of MK 801 and hypothermia used alone and in combination in hypoxic-ischemic brain injury in neonatal rats. Arch Physiol Biochem 2001; 109: 135-144
132. Sanders RD, Ma D, Maze M: Anaesthesia induced neuroprotection. Best Pract Res Clin Anaesthesiol 2005; 19: 461-474
133. Ma D, Williamson P, Januszewski A, Nogaro MC, Hossain M, Ong LP, Shu Y, Franks NP, Maze M: Xenon mitigates isoflurane-induced neurodegeneration in the developing rodent brain. ANESTHESIOLOGY 2007; 10:746-753
134. Martin JL, Ma D, Hossain M, Xu J, Sanders RD, Franks NP, Maze M: Asynchronous administration of xenon and hypothermia significantly reduces brain infarction in the neonatal rat. Br J Anaesth 2007; 98:236-240
135. O'Brien FE, Iwata O, Thornton JS, De Vita E, Sellwood MW, Iwata S, Sakata YS, Charman S, Ordidge R, Cady EB, Wyatt JS, Robertson NJ: Delayed whole-body cooling to 33 or 35 degrees C and the development of impaired energy generation consequential to transient cerebral hypoxia-ischemia in the newborn piglet. Pediatrics 2006; 117:1549-1559
136. Faulkner SD, Kapetanakis A, Bainbridge A, Kato T, DeVita E, Evans S, Cady E, Raivich G, Scaravilli F, Robertson NJ: Neuroprotective effects of xenon, hypothermia, and combined xenon and hypothermia after transient cerebral hypoxia-ischemia in the newborn piglet. E-PAS 2009; 3:2160
137. Siren AL, Fratelli M, Brines M, Goemans C, Casagrande S, Lewczuk P, Keenan S, Gleiter C, Pasquali C, Capobianco A, Mennini T, Heumann R, Cerami A, Ehrenreich H, Ghezzi P: Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci USA 2001; 98:4044-4049
138. Spandou E, Papadopoulou Z, Soubasi V, Karkavelas G, Simeonidou C, Pazaiti A, Guiba-Tziampiri O: Erythropoi-etin prevents long-term sensorimotor deficits and brain injury following neonatal hypoxia-ischemia in rats. Brain Res 2005; 1045:22-30
139. Demers EJ, McPherson RJ, Juul SE: Erythropoietin protects dopaminergic neurons and improves neurobehav-ioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr Res 2005; 58:297-301
140. Ruth V, Autti-Ramo I, Granstrom ML, Korkman M, Raivio KO: Prediction of perinatal brain damage by cord plasma vasopressin, erythropoietin, and hypoxanthine values. J Pediatr 1988; 113:880-885
141. Juul SE, McPherson RJ, Farrell FX, Jolliffe L, Ness DJ, Gleason CA: Erythropoietin concentrations in cerebrospi-nal fluid of nonhuman primates and fetal sheep following high-dose recombinant erythropoietin. Biol Neonate 2004; 85:138-144
142. Zhu C, Kang W, Xu F, Cheng X, Zhang Z, Jia L, Ji L, Guo X, Xiong H, Simbruner G, Blomgren K, Wang X: Erythro-poietin improved neurologic outcomes in newborns with hypoxic-ischemic encephalopathy. Pediatrics 2009; 124: 218-226
143. Niijima S, Shortland DB, Levene MI, Evans DH: Transient hyperoxia and cerebral blood flow velocity in infants born prematurely and at full term. Arch Dis Child 1988; 63:1126-1130
144. Felderhoff-Mueser U, Bittigau P, Sifringer M, Jarosz B, Korobowicz E, Mahler L, Piening T, Moysich A, Grune T, Thor F, Heumann R, Bührer C, Ikonomidou C: Oxygen causes cell death in the developing brain. Neurobiol Dis 2004; 17:273-282
145. Tan A, Schulze A, O'Donnell CP, Davis PG: Air versus oxygen for resuscitation of infants at birth. Cochrane Database Syst Rev 2005; 18:CD002273
146. Rabi Y, Rabi D, Yee W: Room air resuscitation of the depressed newborn: A systematic review and meta-anal-ysis. Resuscitation 2007; 72:353-363
147. Saugstad OD, Ramji S, Soll RF, Vento M: Resuscitation of newborn infants with 21% or 100% oxygen: An updated systematic review and meta-analysis. Neonatology 2008; 94:176-182
148. Karasawa F, Takita A, Fukuda I, Kawatani Y: Nitrous oxide concentrations in maternal and fetal blood during caesarean section. Eur J Anaesthesiol 2003; 20:555-559
149. Peeters-Scholte C, Braun K, Koster J, Kops N, Blomgren K, Buonocore G, van Buul-Offers S, Hagberg H, Nicolay K, van Bel F, Groenendaal F: Effects of allopurinol and deferoxamine on reperfusion injury of the brain in newborn piglets after neonatal hypoxia-ischemia. Pediatr Res 2003; 54:516-522
150. Palmer C, Towfighi J, Roberts RL, Heitjan DF: Allopurinol administered after inducing hypoxia-ischemia reduces brain injury in 7-day-old rats. Pediatr Res 1993; 33:405-411
151. Van Bel F, Shadid M, Moison RM, Dorrepaal CA, Fontijn J, Monteiro L, Van De Bor M, Berger HM: Effect of allopuri-nol on postasphyxial free radical formation, cerebral he-modynamics, and electrical brain activity. Pediatrics 1998; 101:185-193
152. Benders MJ, Bos AF, Rademaker CM, Rijken M, Torrance HL, Groenendaal F, van Bel F: Early postnatal allopurinol does not improve short term outcome after severe birth asphyxia. Arch Dis Child Fetal Neonatal Ed 2006; 91: F163-5
153. Torrance HL, Benders MJ, Derks JB, Rademaker CM, Bos AF, Van Den Berg P, Longini M, Buonocore G, Venegas M, Baquero H, Visser GH, Van Bel F: Maternal allopurinol during fetal hypoxia lowers cord blood levels of the brain injury marker S-100B. Pediatrics 2009; 124:350-357
154. Pei Z, Cheung RT: Pretreatment with melatonin exerts anti-inflammatory effects against ischemia/reperfusion injury in a rat middle cerebral artery occlusion stroke model. J Pineal Res 2004; 37:85-91
155. Pei Z, Pang SF, Cheung RT: Administration of melatonin after onset of ischemia reduces the volume of cerebral infarction in a rat middle cerebral artery occlusion stroke model. Stroke 2003; 4:770-775 (Pubitemid 36307409)
156. Hung YC, Chen TY, Lee EJ, Chen WL, Huang SY, Lee WT, Lee MY, Chen HY, Wu TS: Melatonin decreases matrix metalloproteinase-9 activation and expression and attenuates reperfusion-induced hemorrhage following transient focal cerebral ischemia in rats. J Pineal Res 2008; 45:459-467
157. Husson I, Mesplès B, Bac P, Vamecq J, Evrard P, Gressens P: Melatoninergic neuroprotection of the murine periventricular white matter against neonatal excitotoxic challenge. Ann Neurol 2002; 51:82-92
158. Wang X, Svedin P, Nie C, Lapatto R, Zhu C, Gustavsson M, Sandberg M, Karlsson JO, Romero R, Hagberg H, Mallard C: N-Acetylcysteine reduces lipopolysaccharide-sensi-tized hypoxic-ischemic brain injury. Ann Neurol 2007; 61:263-271
159. Stolp HB, Dziegielewska KM, Ek CJ, Potter AM, Saunders NR: Long-term changes in blood-brain barrier permeability and white matter following prolonged systemic inflammation in early development in the rat. Eur J Neuro-sci 2005; 22:2805-2816
160. Yang D, Nemkul N, Shereen A, Jone A, Dunn RS, Lawrence DA, Lindquist D, Kuan CY: Therapeutic administration of plasminogen activator inhibitor-1 prevents hy-poxic-ischemic brain injury in newborns. J Neurosci 2009; 29:8669-8674
161. Liu XH, Kwon D, Schielke GP, Yang GY, Silverstein FS, Barks JD: Mice deficient in interleukin-1 converting enzyme are resistant to neonatal hypoxic-ischemic brain damage. J Cereb Blood Flow Metab 1999; 19:1099-1108
162. Hedtj̈arn M, Leverin AL, Eriksson K, Blomgren K, Mallard C, Hagberg H: Interleukin-18 involvement in hypoxic-ischemic brain injury. J Neurosci 2002; 22:5910-5919
163. Hagberg H, Gilland E, Bona E, Hanson LA, Hahin-Zoric M, Blennow M, Holst M, McRae A, Söder O: Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxia-ischemia in neonatal rats. Pediatr Res 1996; 40:603-609