The 'pharmacology' of neuronal rescue with cerebral hypothermia

Early Human Development

Volumn 53, Issue 1, 1998, Pages 19-35

  Gunn, Alistair J ^a   Gunn, Tania R ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Fetal sheep; Hypothermia, induced; Hypoxic ischaemic encephalopathy

Indexed keywords

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRAIN EDEMA; BRAIN ISCHEMIA; BRAIN METABOLISM; BRAIN TEMPERATURE; FETUS; HYPOTHERMIA; INDUCED HYPOTHERMIA; MATURATION; NEUROPROTECTION; NONHUMAN; RESUSCITATION; SEIZURE; SHEEP;

ANIMALS; ASPHYXIA NEONATORUM; BRAIN DISEASES; BRAIN ISCHEMIA; HUMANS; HYPOTHERMIA, INDUCED; INFANT, NEWBORN; NEURONS; TIME FACTORS;

EID: 0031725817     PISSN: 03783782     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-3782(98)00033-4     Document Type: Article

References (90)

1. Busto R, Dietrich WD, Globus MY, Valdes I, Scheinberg P, Ginsberg MS. Small differences in intra ischemic brain temperature critically determine the extent of ischemic neuronal injury. J Cereb Blood Flow Metab 1987;7:729-38.
2. Green EJ, Dietrich WD, Van Dijk F, Busto R, Markgraf CG, McCabe PM, Ginsberg MD, Schneiderman N. Protective effects of brain hypothermia on behavior and histopathology following global cerebral ischemia in rats. Brain Res 1992;580:197-204.
3. Nurse S, Corbett D. Direct measurement of brain temperature during and after intraischemic hypothermia: correlation with behavioral, physiological, and histological endpoints. J Neurosci 1994;14:7726-34.
4. Dietrich WD, Busto R, Alonso O, Globus MY, Ginsberg MD. Intraischemic but not postischemic brain hypothermia protects chronically following global forebrain ischemia in rats. J Cereb Blood Flow Metab 1993;13:541-9.
5. Minamisawa H, Smith ML, Siesjö BK. The effect of mild hyperthermia and hypothermia on brain damage following 5, 10, and 15 minutes of forebrain ischemia. Ann Neurol 1990;28:26-33.
6. Laptook AR, Corbett RJT, Sterett R, Burns DK, Tollefsbol G, Garcia D. Modest hypothermia provides partial neuroprotection for ischemic neonatal brain. Pediatr Res 1994;35:436-42.
7. Towfighi J, Housman C, Heitjan DF, Vannucci RC, Yager JY The effect of focal cerebral cooling on perinatal hypoxic-ischemic brain damage. Acta Neuropathol Berlin 1994;87:598-604.
8. Roth SC, Baudin J, Cady E, Johal K, Townsend JP, Wyatt JS, Reynolds EOR, Stewart AL. Relation of deranged neonatal cerebral oxidative metabolism with neurodevelopmental outcome and head circumference at 4 years. Dev Med Child Neurol 1997;39:718-25.
9. Lorek A, Takei Y, Cady EB, Wyatt JS, Penrice J, Edwards AD, Peebles D, Wylezinska M, Owenreece H, Kirkbride V, Cooper CE, Aldridge RF, Roth SC, Brown G, Delpy DT, Reynolds EOR. 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.
10. Thoresen M, Penrice J, Lorek A, Cady EB, Wylezinska M, Kirkbride V, Cooper CE, Brown GC, Edwards AD, Wyatt JS, et al. Mild hypothermia after severe transient hypoxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr Res 1995;37:667-70.
11. Blumberg RM, Cady EB, Wigglesworth JS, Mckenzie JE, Edwards AD. Relation between delayed impairment of cerebral energy metabolism and infarction following transient focal hypoxia-ischaemia in the developing brain. Exp Brain Res 1997;113:130-7.
12. Pulsinelli WA, Brierley JB, Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 1982;11:491-8.
13. Beilharz EJ, Williams CE, Dragunow M, Sirimanne ES, Gluckman PD. Mechanisms of delayed cell death following hypoxic-ischemic injury in the immature rat: evidence for apoptosis during selective neuronal loss. Brain Res 1995;29:1-14.
14. Horn M, Schlote W. Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol Berlin 1992;85:79-87.
15. Dobbing J, Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 1979;3:79-83.
16. Romijn HJ, Hofman MA, Gramsbergen A. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby. Early Hum Dev 1991;26:61-7.
17. Gunn AJ, Gunn TR, de Haan HH, Williams CE, Gluckman PD. Dramatic neuronal rescue with prolonged selective head cooling after ischemia in fetal sheep. J Clin Invest 1997;99:248-56.
18. Williams CE, Gunn AJ, Gluckman PD. The time course of intracellular edema and epileptiform activity following prenatal cerebral ischemia in sheep. Stroke 1991;22:516-21.
19. Tan WKM, Williams CE, During MJ, Mallard CE, Gunning MI, Gunn AJ, Gluckman PD. Accumulation of cytotoxins during the development of seizures and edema after hypoxic-ischemic injury in late gestation fetal sheep. Pediatr Res 1996;39:791-7.
20. Yager J, Towfighi J, Vannucci RC. Influence of mild hypothermia on hypoxic-ischemic brain damage in the immature rat. Pediatr Res 1993;34:525-9.
21. Thoresen M, Bagenholm R, Loberg EM, Apricena F, Kjellmer I. Posthypoxic cooling of neonatal rats provides protection against brain injury. Arch Dis Child Fetal Neonat Ed 1996;74:F1-7.
22. Trescher WH, Ishiwa S, Johnston MV. Brief post-hypoxic-ischemic hypothermia markedly delays neonatal brain injury. Brain Dev 1997;19:326-38.
23. Haaland K, Loberg EM, Steen PA, Thoresen M. Posthypoxic hypothermia in newborn piglets. Pediatr Res 1997;41:505-12.
24. Laptook AR, Corbett RJT, Sterett R, Burns DK, Garcia D, Tollefsbol G. Modest hypothermia provides partial neuroprotection when used for immediate resuscitation after brain ischemia. Pediatr Res 1997;42:17-23.
25. Iwai T, Niwa M, Yamada H, Nozaki M, Tsurumi K. Hypothermic prevention of the hippocampal damage following ischemia in Mongolian gerbils comparison between intraischemic and brief postischemic hypothermia. Life Sci 1993;52:1031-8.
26. Busto R, Dietrich WD, Globus MY, Ginsberg MD. Postischemic moderate hypothermia inhibits CA1 hippocampal ischemic neuronal injury. Neurosci Lett 1989;101:299-304.
27. Shuaib A, Trulove D, Ijaz MS, Kanthan R, Kalra J. The effect of post-ischemic hypothermia following repetitive cerebral ischemia in gerbils. Neurosci Lett 1995;186:165-8.
28. Horn M, Schlote W, Henrich HA. Global cerebral ischemia and subsequent selective hypothermia. A neuropathological and morphometrical study on ischemic neuronal damage in cat. Acta Neuropathol Berlin 1991;81:443-9.
29. Kuboyama K, Safar P, Radovsky A, Tisherman SA, Stezoski SW, Alexander H. Delay in cooling negates the beneficial effect of mild resuscitative cerebral hypothermia after cardiac arrest in dogs: a prospective, randomized study. Crit Care Med 1993;21:1348-58.
30. Chopp M, Chen H, Dereski MO, Garcia JH. Mild hypothermic intervention after graded ischemic stress in rats. Stroke 1991;22:37-43.
31. Coimbra C, Drake M, Boris-Moller F, Wieloch T. Long-lasting neuroprotective effect of postischemic hypothermia and treatment with an anti-inflammatory/antipyretic drug. Evidence for chronic encephalopathic processes following ischemia. Stroke 1996;27:1578-85.
32. Colbourne F, Corbett D. Delayed and prolonged post-ischemic hypothermia is neuroprotective in the gerbil. Brain Res 1994;654:265-72.
33. Zhao W, Richardson JS, Mombourquette MJ, Weil JA, Ijaz S, Shuaib A. Neuroprotective effects of hypothermia and U-78517f in cerebral ischemia are due to reducing oxygen-based free radicals - an electron paramagnetic resonance study with gerbils. J Neurosci Res 1996;45:282-8.
34. Carroll M, Beek O. Protection against hippocampal CA1 cell loss by post-ischemic hypothermia is dependent on delay of initiation and duration. Metab Brain Dis 1992;7:45-50.
35. Coimbra C, Wieloch T. Moderate hypothermia mitigates neuronal damage in the rat brain when initiated several hours following transient cerebral ischemia. Acta Neuropathol Berlin 1994;87:325-31.
36. Sirimanne ES, Blumberg RM, Bossano D, Gunning MI, Edwards AD, Gluckman PD, Williams CE. The effect of prolonged modification of cerebral temperature on outcome following hypoxic ischemic injury in the infant rat. Pediatr Res 1996;39:591-8.
37. Yanamoto H, Hong SC, Soleau S, Kassell NF, Lee KS. Mild postischemic hypothermia limits cerebral injury following transient focal ischemia in rat neocortex. Brain Res 1996;718:207-11.
38. Edwards AD, Yue X, Squier MV, Thoresen M, Cady EB, Penrice J, Cooper CE, Wyatt JS, Reynolds EO, Mehmet H. Specific inhibition of apoptosis after cerebral hypoxia-ischaemia by moderate post-insult hypothermia. Biochem Biophys Res Commun 1995;217:1193-9.
39. Gunn TR, Gunn AJ, Gluckman PD. Substantial neuronal rescue with prolonged selective head cooling begun 5.5 h after cerebral ischemia in the fetal sheep. Pediatr Res 1997;41:898A.
40. Nurse S, Corbett D. Neuroprotection after several days of mild, drug-induced hypothermia. J Cereb Blood Flow Metab 1996;16:474-80.
41. Colbourne F, Corbett D. Delayed postischemic hypothermia: a six month survival study using behavioral and histological assessments of neuroprotection. J Neurosci 1995;15:7250-60.
42. Colbourne F, Sutherland G, Corbett D. Postischemic hypothermia - A critical appraisal with implications for clinical treatment. Mol Neurobiol 1997;14:171-201.
43. Marion DW, Penrod LE, Kelsey SF, Obrist WD, Kochanek PM, Palmer AMX, Wisniewski SR, DeKosky ST. Treatment of traumatic brain injury with moderate hypothermia. New Engl J Med 1997;336:540-6.
44. Weinrauch V, Safar P, Tisherman S, Kuboyama K, Radovsky A. Beneficial effect of mild hypothermia and detrimental effect of deep hypothermia after cardiac arrest in dogs. Stroke 1992;23:1454-62.
45. Leonov Y, Sterz F, Safar P, Radovsky A. Moderate hypothermia after cardiac arrest of 17 minutes in dogs. Effect on cerebral and cardiac outcome. Stroke 1990;21:1600-6.
46. Safar P, Xiao F, Radovsky A, Tanigawa K, Ebmeyer U, Bircher NG, Alexander H, Stezoski SW. Improved cerebral resuscitation from cardiac arrest in dogs with mild hypothermia plus blood flow promotion. Stroke 1996;27:105-13.
47. Greene PS, Cameron DE, Mohlala ML, Dinatale JM, Gardner TJ. Systolic and diastolic left ventricular dysfunction due to mild hypothermia. Circulation 1989;80:III44-8.
48. Dudgeon DL, Randall PA, Hill RB, McAfee JG. Mild hypothermia: its effect on cardiac output and regional perfusion in the neonatal piglet. J Pediatr Surg 1980;15:805-10.
49. Gunn AJ, de Haan HH, Maxwell L, Gunn TR, Williams CE, Gluckman PD. Does myocardial stunning contribute to cardiac dysfunction after intermittent severe asphyxia in the fetal lamb?. Pediatr Res (Abstr) 1997;41:897A.
50. de Haan HH, Gunn AJ, Gluckman PD. Experiments in perinatal brain injury: What have we learnt?. Prenatal Neonatal Med 1996;1:16-25.
51. Low JA, Froese AB, Galbraith RS, Smith JT, Sauerbrei EE, Derrick EJ. The association between preterm newborn hypotension and hypoxemia and outcome during the first year. Acta Paediatr Scand 1993;82:433-7.
52. Baena RC, Busto R, Dietrich WD, Globus MY, Ginsberg MD. Hyperthermia delayed by 24 hours aggravates neuronal damage in rat hippocampus following global ischemia. Neurology 1997;48:768-73.
53. Kim Y, Busto R, Dietrich WD, Kraydieh S, Ginsberg MD. Delayed postischemic hyperthermia in awake rats worsens the histopathological outcome of transient focal cerebral ischemia. Stroke 1996;27:2274-80.
54. Corbett D, Nurse S, Colbourne F. Hypothermic neuroprotection - a global ischemia study using 18- to 20-month-old gerbils. Stroke 1997;28:2238-42.
55. 1H magnetic resonance spectroscopy. Pediatr Res 1995;38:919-25.
56. Bruno VMG, Goldberg MP, Dugan LL, Giffard RG, Choi DW Neuroprotective effect of hypothermia in cortical cultures exposed to oxygen-glucose deprivation or excitatory amino acids. J Neurochem 1994;63:1398-406.
57. Busto R, Globus MY, Dietrich WD, Martinez E, Valdes I, Ginsberg MD. Effect of mild hypothermia on ischemia-induced release of neurotransmitters and free fatty acids in rat brain. Stroke 1989;20:904-10.
58. Nakashima K, Todd MM. Effects of hypothermia, pentobarbital, and isoflurane on postdepolarization amino acid release during complete global cerebral ischemia. Anesthesiology 1996;85:161-8.
59. Kader A, Frazzini VI, Baker CJ, Solomon RA, Trifiletti RR. Effect of mild hypothermia on nitric oxide synthesis during focal cerebral ischemia. Neurosurgery 1994;35:272-7.
60. Lei BP, Adachi N, Arai T. The effect of hypothermia on H2O2 production during ischemia and reperfusion - a microdialysis study in the gerbil hippocampus. Neurosci Lett 1997;222:91-4.
61. Bagenholm R, Nilsson UA, Gotborg CW, Kjellmer I. Free radicals are formed in the brain of fetal sheep during reperfusion after cerebral ischemia. Pediatr Res 1998;43:271-5.
62. Bagenholm R, Nilsson UA, Kjellmer I. Formation of free radicals in hypoxic ischemic brain damage in the neonatal rat, assessed by an endogenous spin trap and lipid peroxidation. Brain Res 1997;773:132-8.
63. Lei B, Tan X, Cai H, Xu Q, Guo Q. Effect of moderate hypothermia on lipid peroxidation in canine brain tissue after cardiac arrest and resuscitation. Stroke 1994;25:147-52.
64. Thoresen M, Satas S, Pukasundvall M, Whitelaw A, Hallstrom A, Loberg EM, Ungerstedt U, Steen PA, Hagberg H. Post-hypoxic hypothermia reduces cerebrocortical release of NO and excitotoxins. NeuroReport 1997;8:3359-62.
65. Globus MYT, Alonso O, Dietrich WD, Busto R, Ginsberg MD. Glutamate release and free radical production following brain injury - effects of posttraumatic hypothermia. J Neurochem 1995;65:1704-11.
66. Palmer AM, Marion DW, Botscheller ML, Redd EE. Therapeutic hypothermia is cytoprotective without attenuating the traumatic brain injury-induced elevations in interstitial concentrations of aspartate and glutamate. J Neurotrauma 1993;10:363-72.
67. Tan WKM, Williams CE, Gunn AJ, Mallard EC, Gluckman PD. Suppression of postischemic epileptiform activity with MK-801 improves neural outcome in fetal sheep. Ann Neurol 1992;32:677-82.
68. Van Bel F, Dorrepaal CA, Benders MJ, Zeeuwe PE, van de Bor M, Berger HM. Changes in cerebral hemodynamics and oxygenation in the first 24 hours after birth asphyxia. Pediatrics 1993;92:365-72.
69. Nevander G, Ingvar M, Auer RN, Siesjö BK. Status epilepticus in well-oxygenated rats causes neuronal necrosis. Ann Neurol 1985;18:281-90.
70. Takaoka S, Pearlstein RD, Warner DS. Hypothermia reduces the propensity of cortical tissue to propagate direct current depolarizations in the rat. Neurosci Lett 1996;218:25-8.
71. Hossmann KA. Glutamate-mediated injury in focal cerebral ischemia - the excitotoxin hypothesis revised. Brain Pathol 1994;4:23-36.
72. Zeevalk GD, Nicklas WJ. Hypothermia and metabolic stress-narrowing the cellular site of early neuroprotection. J Pharmacol Exp Ther 1996;279:332-9.
73. Kristian T, Katsura K, Siesjö BK. The influence of moderate hypothermia on cellular calcium uptake in complete ischaemia: implications for the excitotoxic hypothesis. Acta Physiol Scand 1992;146:531-2.
74. Shuaib A, Sochocka E, Code W, Hertz L. Hypothermia protects astrocytes during ischemia in cell culture. Neurosci Lett 1992;146:69-71.
75. Gottron FJ, Ying HS, Choi DW. Caspase inhibition selectively reduces the apoptotic component of oxygen-glucose deprivation-induced cortical neuronal cell death. Mol Cell Neurosci 1997;9:159-69.
76. Markgraf CG, Velayo NL, Johnson MP, McCarty DR, Medhi S, Koehl JR, Chmielewski PA, Linnik MD. Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. Stroke 1998;29:152-8.
77. Rothwell NJ, Strijbos PJLM. Cytokines in neurodegeneration and repair. Int J Dev Neurosci 1995;13:179-85.
78. Silverstein FS, Barks JDE, Hagan P, Liu XH, Ivacko J, Szaflarski J. Cytokines and perinatal brain injury. Neurochem Int 1997;30:375-83.
79. Goss JR, Styren SD, Miller PD, Kochanek PM, Palmer AM, Marion DW, DeKosky ST. Hypothermia attenuates the normal increase in interleukin 1 beta RNA and nerve growth factor following traumatic brain injury in the rat. J Neurotrauma 1995;12:159-67.
80. Martin D, Chinookoswong N, Miller G. The interleukin-1 receptor antagonist (rhIL-1ra) protects against cerebral infarction in a rat model of hypoxia-ischemia. Exp Neurol 1994;130:362-7.
81. Stroemer RP, Rothwell NJ. Cortical protection by localized striatal injection of IL-1ra following cerebral ischemia in the rat. J Cereb Blood Flow Metab 1997;17:597-604.
82. Nagata S. Fas-mediated apoptosis. Adv Exp Med Biol 1996;406:119-24.
83. Schwartz LM, Milligan CE. Cold thoughts of death: the role of ICE proteases in neuronal cell death. Trends Neurosci 1996;19:555-62.
84. Gwag BJ, Koh JY, Demaro JA, Ying HS, Jacquin M, Choi DW Slowly triggered excitotoxicity occurs by necrosis in cortical cultures. Neuroscience 1997;77:393-401.
85. McDonald JW, Behrens MI, Chung C, Bhattacharyya T, Choi DW Susceptibility to apoptosis is enhanced in immature cortical neurons. Brain Res 1997;759:228-32.
86. Silverman WA, Fertig JW, Berger PA. The influence of the thermal environment upon the survival of newly born premature infants. Pediatrics 1958;31:876-85.
87. Schubert A. Side effects of mild hypothermia. J Neurosurg Anesthesiol 1995;7:139-47.
88. Gunn AJ, Gunn TR. Effect of radiant heat on head temperature gradient in term infants. Arch Dis Child Fetal Neonat Ed 1996;74:F200-3.
89. Schwab S, Spranger M, Aschoff A, Steiner T, Hacke W. Brain temperature monitoring and modulation in patients with severe MCA infarction. Neurology 1997;48:762-7.
90. Gelman B, Schleien CL, Lohe A, Kuluz JW. Selective brain cooling in infant piglets after cardiac arrest and resuscitation. Crit Care Med 1996;24:1009-17.