Therapeutic hypothermia as a neuroprotective strategy in neonatal hypoxic-ischemic brain injury and traumatic brain injury

Current Molecular Medicine

Volumn 12, Issue 10, 2012, Pages 1282-1296

  Ma, H ^a   Sinha, B ^b   Pandya, R S ^b   Lin, N ^b   Popp, A J ^b   Li, J ^a   Yao, J ^a   Wang, X ^b  

^a GUANGXI MEDICAL UNIVERSITY   (China)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Apoptosis; Hypothermia; Hypoxic ischemic encephalopathy; Neonatal hypoxic ischemic brain injury; Neuroprotection; Traumatic brain injury

Indexed keywords

C REACTIVE PROTEIN; CALPAIN; CASPASE 2; CASPASE 3; CASPASE 8; CASPASE 9; CREATINE PHOSPHATE; CYTOCHROME C; GELATINASE B; GLUCOSE; GLUTAMIC ACID; INTERLEUKIN 10; INTERLEUKIN 11; INTERLEUKIN 6; INTERLEUKIN 8; LACTIC ACID; MICROTUBULE ASSOCIATED PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NITRIC OXIDE; PHOSPHATE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ANTIOXIDANT ACTIVITY; APOPTOSIS; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN EDEMA; BRAIN TEMPERATURE; CELL DEATH; ENERGY METABOLISM; EXCITOTOXICITY; GENE EXPRESSION; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INDUCED HYPOTHERMIA; INFLAMMATION; META ANALYSIS (TOPIC); MORTALITY; NEUROPROTECTION; NEWBORN HYPOXIA; NONHUMAN; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; THERAPY EFFECT; TRAUMATIC BRAIN INJURY;

ADULT; APOPTOSIS; BRAIN; BRAIN INJURIES; HUMANS; HYPOTHERMIA, INDUCED; HYPOXIA-ISCHEMIA, BRAIN; INFANT, NEWBORN; INFLAMMATION MEDIATORS; NEUROPROTECTIVE AGENTS; NEUROTRANSMITTER AGENTS; REACTIVE OXYGEN SPECIES;

EID: 84870202240     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/156652412803833517     Document Type: Review

References (126)

1. Ginsberg MD, Sternau LL, Globus MY, Dietrich WD, Busto R. Therapeutic modulation of brain temperature: relevance to ischemic brain injury. Cerebrovasc Brain Metab Rev 1992; 4: 189-225.
2. Smith LW, Fay T. Observations on human beings with cancer, maintained at reduced temperatures of 75-90 °F. Am J Clin Pathol 1940; 10: 1-11.
3. Fay T. Observations on prolonged human refrigeration. N Y State J Med 1940; 40: 1351-1354.
4. Fay T. Observations on generalized refrigeration in cases of severe cerebral trauma. Assoc Res Nerv Ment Dis Proc 1943; 24: 611-619.
5. Spencer FC, Bahnson HT. The present role of hypothermia in cardiac surgery. Circulation 1962; 26: 292-300.
6. Botterell EH, Lougheed WM, Morley TP, Vandewater SL. Hypothermia in the surgical treatment of ruptured intracranial aneurysms. J Neurosurg1958; 15: 4-18.
7. Sahuquillo J, Vilalta A. Cooling the injured brain: how does moderate hypothermia influence the pathophysiology of traumatic brain injury. Curr Pharm Des 2007; 13: 2310-2322.
8. Jenkins LW, DeWitt DS, Johnston WE, Davis KL, Prough DS. Intraischemic mild hypothermia increases hippocampal CA1 blood flow during forebrain ischemia. Brain Res 2001; 890: 1-10.
9. Sick TJ, Tang R, Perez-Pinzon MA. Cerebral blood flow does not mediate the effect of brain temperature on recovery of extracellular potassium ion activity after transient focal ischemia in the rat. Brain Res 1999; 821: 400-406.
10. Erecinska M, Thoresen M, Silver IA. Effects of hypothermia on energy metabolism in Mammalian central nervous system. J Cereb Blood Flow Metab 2003; 23: 513-530.
11. Globus MY, Busto R, Dietrich WD, Martinez E, Valdes I, Ginsberg MD. Effect of ischemia on the in vivo release of striatal dopamine, glutamate, and gamma-aminobutyric acid studied by intracerebral microdialysis. J Neurochem1988; 51: 1455-1464.
12. Okuda C, Saito A, Miyazaki M, Kuriyama K. Alteration of the turnover of dopamine and 5-hydroxytryptamine in rat brain associated with hypothermia. Pharmacol Biochem Behav 1986; 24: 79-83.
13. Lei B, 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: 91-94.
14. Guven H, Amanvermez R, Malazgirt Z, et al. Moderate hypothermia prevents brain stem oxidative stress injury after hemorrhagic shock. J Trauma 2002; 53: 66-72.
15. Globus MY, 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: 1704-1711.
16. Vannucci RC. Experimental biology of cerebral hypoxiaischemia: relation to perinatal brain damage. Pediatr Res 1990; 27: 317-326.
17. Dilenge ME, Majnemer A, Shevell MI. Long-term developmental outcome of asphyxiated term neonates. J Child Neurol 2001; 16: 781-792.
18. Graham WJ, Ahmed S, Stanton C, Abou-Zahr C, Campbell OM. Measuring maternal mortality: an overview of opportunities and options for developing countries. BMC Med 2008; 6: 12.
19. Airede AI. Birth asphyxia and hypoxic-ischaemic encephalopathy: incidence and severity. Ann Trop Paediatr 1991; 11: 331-335.
20. Wang X, Panyda R, Yao J, Ma H, Li J. Targeting caspases in neonatal hypoxia-ischemic brain injury and traumatic brain injury. Neurodegeneration: Theory, Disorders and Treatments. McNeill AS, Ed. NOVA Science Publishers Inc New York 2010; pp. 125-134.
21. Lorek A, Takei Y, Cady EB, et al. 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.
22. Perlman JM. Intervention strategies for neonatal hypoxicischemic cerebral injury. Clin Ther 2006; 28: 1353-1365.
23. Laptook AR, Corbett RJ, Ruley J, Olivares E. Blood flow and metabolism during and after repeated partial brain ischemia in neonatal piglets. Stroke 1992; 23: 380-387.
24. Adams H, Mitchell DE, Graham DI, Doyle, D. Diffuse brain damage of immediate impact type. Its relationship to 'primary brain-stem damage' in head injury. Brain 1977; 100: 489-502.
25. Graham DI, Adams JH, Gennarelli TA. Pathology of brain damage in head injury. In: Cooper PR, Ed. Head injury. Baltimore: Williams and Wilkins 1987; pp. 72-88.
26. Pitts LH, Mcintosh TK. Dynamic changes after brain trauma. In: Braakman R, Ed. Handbook of Clinical Neurology. Head Injury. Amsterdam: Elsevier Science Publishers BV 1990; Vol. 13 (57): pp. 65-100.
27. Petrov T, Page AB, Owen CR, Rafols JA. Expression of the inducible nitric oxide synthase in distinct cellular types after traumatic brain injury: an in situ hybridization and immunocytochemical study Acta. Neuropathol 2000; 100: 196-204.
28. Yao J, Zeng X, Zhang J. Research change and anlysis of endothelins in the plasma of patients after severe head injury. Guangxi Medical Journal 1999; 21: 63-65.
29. Teasdale GM, Graham DI. Craniocerebral trauma: protection and retrieval of the neuronal population after injury. Neurosurgery 1998; 43: 723-737; discussion 737-8.
30. Bramlett HM, Dietrich WD, Green EJ, Busto R. Chronic histopathological consequences of fluid-percussion brain injury in rats: effects of post-traumatic hypothermia. Acta Neuropathol 1997; 93: 190-199.
31. Vialard PL, Z Navarranne. [Two cases of severe cerebral concussion treated and cured by artificial hibernation]. Anesth Anal 1954; 11: 431-436.
32. Mayrhofer O, Kuhlmayer R. [Artificial hypothermia (hibernation) as supporting measure in the treatment of severe cranium trauma].Wien Klin Wochenschr 1954; 66: 495-497.
33. Wang Q, Li AL, Zhi DS, Huang HL. Effect of mild hypothermia on glucose metabolism and glycerol of brain tissue in patients with severe traumatic brain injury. Chin J Traumatol 2007;10: 246-249.
34. Kimberger O, Kurz A. Thermoregulatory management for mild therapeutic hypothermia. Best Pract Res Clin Anaesthesiol 2008; 22: 729-744.
35. Christian E, Zada G, Sung G, Giannotta SL. A review of selective hypothermia in the management of traumatic brain injury. Neurosurg Focus 2008; 25: E9.
36. Feng JF, Zhang KM, Jiang JY, Gao GY, Fu X, Liang YM. Effect of therapeutic mild hypothermia on the genomics of the hippocampus after moderate traumatic brain injury in rats. Neurosurgery 2010; 67(3): 730-742.
37. Adamchik Y, Frantseva MV, Weisspapir M, Carlen PL, Perez Velazquez JL. Methods to induce primary and secondary traumatic damage in organotypic hippocampal slice cultures. Brain Res Brain Res Protoc 2000; 5: 153-158.
38. Newman GC, Qi H, Hospod FE, Grundmann K. Preservation of hippocampal brain slices with in vivo or in vitro hypothermia. Brain Res 1992; 575: 159-163.
39. Rossaint J, Rossaint R, Weis J, Fries M, Rex S, Coburn M. Propofol: neuroprotection in an in vitro model of traumatic brain injury. Crit Care 2009; 13: R61.
40. Sakai F, Amaha K. The effects of hypothermia on a cloned human brain glutamate transporter (hGLT-1) expressed in Chinese hamster ovary cells: -[3H]L-glutamate uptake study. Anesth Analg 1999; 89: 1546-1550.
41. Johnston MV, Trescher WH, Ishida A, Nakajima W. Neurobiology of hypoxic-ischemic injury in the developing brain. Pediatr Res 2001; 49: 735-741.
42. Siesjo BK, Bengtsson F. Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J Cereb Blood Flow Metab 1989; 9: 127-140.
43. Jacobson MD. Programmed cell death: a missing link is found. Trends Cell Biol 1997; 7: 467-469.
44. Edwards AD, Yue X, Squier MV, et al. Specific inhibition of apoptosis after cerebral hypoxia-ischaemia by moderate post-insult hypothermia. Biochem Biophys Res Commun 1995; 217: 1193-1199.
45. Rothstein RP, Levison SW. Gray matter oligodendrocyte progenitors and neurons die caspase-3 mediated deaths subsequent to mild perinatal hypoxic/ischemic insults. Dev Neurosci 2005; 27: 149-159.
46. Ohmura A, Nakajima W, Ishida A, et al. Prolonged hypothermia protects neonatal rat brain against hypoxicischemia by reducing both apoptosis and necrosis. Brain Dev 2005; 27: 517-526.
47. Zhu C, Wang X, Cheng X, et al. Post-ischemic hypothermiainduced tissue protection and diminished apoptosis after neonatal cerebral hypoxia-ischemia. Brain Res 2004; 996: 67-75.
48. Liu CQ, Xia YF, Yuan YX, Li L, Qiu XL. [Effects of selective head cooling with mild hypothermia on serum levels of caspase-3 and IL-18 in neonates with hypoxic-ischemic encephalopathy]. Zhongguo Dang Dai Er Ke Za Zhi 2010; 12: 690-692.
49. Wang LS, Yu LJ, Shao XM. [Mild hypothermia attenuates neuronal apoptosis after cerebral hypoxia-ischemia in neonatal rats]. Zhongguo Dang Dai Er Ke Za Zhi 2007; 9: 37-41.
50. Tomimatsu T, Fukuda H, Endo M, et al. Effects of hypothermia on neonatal hypoxic-ischemic brain injury in the rat: phosphorylation of Akt, activation of caspase-3-like protease. Neurosci Lett 2001; 312: 21-24.
51. Ogihara T, Hirano K, Ogihara H, et al. Non-protein-bound transition metals and hydroxyl radical generation in cerebrospinal fluid of newborn infants with hypoxic ischemic encephalopathy. Pediatr Res 2003; 53: 594-599.
52. Hiroi M, Ogihara T, Hirano K, et al. Regulation of apoptosis by glutathione redox state in PC12 cells exposed simultaneously to iron and ascorbic acid. Free Radic Biol Med 2005; 38: 1057-1072.
53. Hasegawa M, Ogihara T, Tamai H, Hiroi M. Hypothermic inhibition of apoptotic pathways for combined neurotoxicity of iron and ascorbic acid in differentiated PC12 cells: reduction of oxidative stress and maintenance of the glutathione redox state. Brain Res 2009; 1283: 1-13.
54. Matsui T, Kakeda T. IL-10 production is reduced by hypothermia but augmented by hyperthermia in rat microglia. J Neurotrauma 2008; 25: 709-715.
55. 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: 351-357.
56. Perrone S, Szabo M, Bellieni CV, et al. Whole body hypothermia and oxidative stress in babies with hypoxicischemic brain injury. Pediatr Neurol 2010; 43: 236-240.
57. 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: 67-76.
58. Yager JY, Asselin J. Effect of mild hypothermia on cerebral energy metabolism during the evolution of hypoxic-ischemic brain damage in the immature rat. Stroke 1996; 27: 919-925; discussion 926.
59. O'Brien FE, Iwata O, Thornton JS, et al. 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.
60. Dietrich WD. Therapeutic hypothermia in experimental models of traumatic brain injury. In: Hayashi N, Ed. Brain Hypothermia. Hayashi N Ed. Brain Hypothermia. Tokyo: Springer-Verlag. 2000; pp. 39-46.
61. McCarthy MM. Stretching the truth. Why hippocampal neurons are so vulnerable following traumatic brain injury. Exp Neurol 2003; 184: 40-43.
62. Clausen F, Lundqvist H, Ekmark S, Lewen A, Ebendal T, Hillered L. Oxygen free radical-dependent activation of extracellular signal-regulated kinase mediates apoptosis-like cell death after traumatic brain injury. J Neurotrauma 2004; 21: 1168-1182.
63. Huang T, Solano J, He D, Loutfi M, Dietrich W D, Kuluz JW. Traumatic injury activates MAP kinases in astrocytes: mechanisms of hypothermia and hyperthermia. J Neurotrauma 2009; 26: 1535-1545.
64. Lotocki G, de Rivero Vaccari JP, Perez ER, et al. Therapeutic hypothermia modulates TNFR1 signaling in the traumatized brain via early transient activation of the JNK pathway and suppression of XIAP cleavage. Eur J Neurosci 2006; 24: 2283-2290.
65. Sui LS, Han F, Guo YW, et al. [Time course of calpain activity changes in rat neurons following fluid percussion injury and the interventional effect of mild hypothermia]. Nan Fang Yi Ke Da Xue Xue Bao 2007; 27: 1149-1151.
66. Jia F, Jiang JY, Liang YM, Mao Q. The effect of hypothermia on the expression of TIMP-3 after traumatic brain injury in rats. J Neurotrauma 2009; [Epub ahead of print].
67. Haranishi Y, Kawata R, Fukuda S, et al. Moderate hypothermia, but not calpain inhibitor 2, attenuates the proteolysis of microtubule-associated protein 2 in the hippocampus following traumatic brain injury in rats. Eur J Anaesthesiol 2005; 22: 140-147.
68. Shein NA, Doron H, Horowitz M, et al. Altered cytokine expression and sustained hypothermia following traumatic brain injury in heat acclimated mice. Brain Res 2007; 1185: 313-320.
69. Mitchell HM, White DM, Domowicz MS, Kraig RP. Cold preconditioning neuroprotection depends on TNF-alpha and is enhanced by blockade of interleukin-11. J Neurochem 2011; 117: 187-196.
70. Suehiro E, Fujisawa H, Akimura T, et al. Increased matrix metalloproteinase-9 in blood in association with activation of interleukin-6 after traumatic brain injury: influence of hypothermic therapy. J Neurotrauma 2004; 21: 1706-1711.
71. Bayir H, Marion DW, Puccio AM, et al. Marked gender effect on lipid peroxidation after severe traumatic brain injury in adult patients. J Neurotrauma 2004; 21: 1-8.
72. Bruno VM, 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 Neurochem1994; 63: 1398-1406.
73. Ooba S, Hasuo H, Shigemori M, Yamashita S, Akasu T. Mild hypothermia prevents post-traumatic hyperactivity of excitatory synapses in rat hippocampal CA1 pyramidal neurons. Kurume Med J 2009; 56: 49-59.
74. Stahel PF, Shohami E, Younis FM, et al. Experimental closed head injury: analysis of neurological outcome, bloodbrain barrier dysfunction, intracranial neutrophil infiltration, and neuronal cell death in mice deficient in genes for proinflammatory cytokines. J Cereb Blood Flow Metab 2000; 20: 369-380.
75. Korn A, Golan H, Melamed I, Pascual-Marqui R, Friedman A. Focal cortical dysfunction and blood-brain barrier disruption in patients with Postconcussion syndrome. J Clin Neurophysiol 2005; 22: 1-9.
76. Jiang JY, Lyeth BG, Kapasi MZ, Jenkins LW, Povlishock JT. Moderate hypothermia reduces blood-brain barrier disruption following traumatic brain injury in the rat. Acta Neuropathol 1992; 84: 495-500.
77. Lotocki G, Vaccari JP, Perez ER, et al. Alterations in bloodbrain barrier permeability to large and small molecules and leukocyte accumulation after traumatic brain injury: effects of post-traumatic hypothermia. J Neurotrauma 2009; 26: 1123-1134.
78. Szczygielski J, Mautes AE, Schwerdtfeger K, Steudel WI. The effects of selective brain hypothermia and decompressive craniectomy on brain edema after closed head injury in mice. Acta Neurochir Suppl 2010; 106: 225-229.
79. Polderman KH. Application of therapeutic hypothermia in the ICU: opportunities and pitfalls of a promising treatment modality. Part 1: Indications and evidence Posttraumatic hypothermia followed by slow rewarming protects the cerebral microcirculation. Intensive Care Med 2004; 30: 556-575.
80. Suehiro E, Ueda Y, Wei EP, Kontos HA, Povlishock JT. Posttraumatic hypothermia followed by slow rewarming protects the cerebral microcirculation. J Neurotrauma 2003; 20: 381-390.
81. Oda Y, Gao G, Wei EP, Povlishock JT. Combinational therapy using hypothermia and the immunophilin ligand FK506 to target altered pial arteriolar reactivity, axonal damage, and blood-brain barrier dysfunction after traumatic brain injury in rat. J Cereb Blood Flow Metab 2011; 4: 1143-1154.
82. Azzopardi D, Brocklehurst P, Edwards D, et al. The TOBY Study. Whole body hypothermia for the treatment of perinatal asphyxial encephalopathy: a randomised controlled trial. BMC Pediatr. 2008; 8: 17.
83. Gunn AJ, Gluckman PD, Gunn TR. Selective head cooling in newborn infants after perinatal asphyxia: a safety study. Pediatrics1998; 102: 885-892.
84. Thoresen M, Satas S, Puka-Sundvall M, et al. Post-hypoxic hypothermia reduces cerebrocortical release of NO and excitotoxins. Neuroreport 1997; 8: 3359-3362.
85. Fukuda H, Tomimatsu T, Watanabe N, et al. Post-ischemic hypothermia blocks caspase-3 activation in the newborn rat brain after hypoxia-ischemia. Brain Res 2001; 910: 187-191.
86. Zanelli SA, Naylor M, Dobbins N, et al. Implementation of a 'Hypothermia for HIE' program: 2-year experience in a single NICU. J Perinatol 2008; 28: 171-175.
87. Laptook AR, Corbett RJ, Burns D, Sterett R. Neonatal ischemic neuroprotection by modest hypothermia is associated with attenuated brain acidosis. Stroke1995; 26: 1240-1246.
88. Rutherford MA, Azzopardi D, Whitelaw A, et al. Mild hypothermia and the distribution of cerebral lesions in neonates with hypoxic-ischemic encephalopathy. Pediatrics 2005; 116: 1001-1006.
89. Laptook AR, Shalak L, Corbett RJ. Differences in brain temperature and cerebral blood flow during selective head versus whole-body cooling. Pediatrics 2001; 108: 1103-1110.
90. Thoresen M, Simmonds M, Satas S, Tooley J, Silver IA. Effective selective head cooling during posthypoxic hypothermia in newborn piglets. Pediatr Res 2001; 49: 594-599.
91. Shah PS, Ohlsson A, Perlman M. Hypothermia to treat neonatal hypoxic ischemic encephalopathy: systematic review. Arch Pediatr Adolesc Med 2007; 161: 951-958.
92. Gluckman PD, Wyatt JS, Azzopardi D, et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet 2005; 365: 663-670.
93. Shankaran S, Laptook A, Wright LL, et al. Whole-body hypothermia for neonatal encephalopathy: animal observations as a basis for a randomized, controlled pilot study in term infants. Pediatrics 2002; 110: 377-385.
94. Eicher DJ, Wagner CL, Katikaneni LP, et al. Moderate hypothermia in neonatal encephalopathy: efficacy outcomes. Pediatr Neurol 2005; 32: 11-17.
95. Azzopardi D, Strohm B, Edwards AD, et al. Treatment of asphyxiated newborns with moderate hypothermia in routine clinical practice: how cooling is managed in the UK outside a clinical trial. Arch Dis Child Fetal Neonatal Ed 2009; 94: F260-F264.
96. Laptook A, Tyson J, Shankaran S, et al. Elevated temperature after hypoxic-ischemic encephalopathy: risk factor for adverse outcomes. Pediatrics 2008; 122: 491-499.
97. Wyatt J S, Gluckman P D, Liu P Y, et al. Determinants of outcomes after head cooling for neonatal encephalopathy. Pediatrics 2007; 119: 912-921.
98. Shiozaki T, Sugimoto H, Taneda M, et al. Effect of mild hypothermia on uncontrollable intracranial hypertension after severe head injury. J Neurosurg 1993; 79: 363-368.
99. Clifton GL, Allen S, Barrodale P, et al. A phase II study of moderate hypothermia in severe brain injury. J Neurotrauma 1993; 10: 263-271; discussion 273.
100. Marion DW, Penrod LE, Kelsey SF, et al. Treatment of traumatic brain injury with moderate hypothermia. N Engl J Med 1997; 336: 540-546.
101. Narayan RK. Hypothermia for traumatic brain injury--a good idea proved ineffective. N Engl J Med 2001; 344: 602-603.
102. Clifton GL, Miller ER, Choi SC, et al. Lack of effect of induction of hypothermia after acute brain injury. N Engl J Med 2001; 344: 556-563.
103. Hutchison JS, Ward RE, Lacroix J, et al. Hypothermia therapy after traumatic brain injury in children. N Engl J Med 2008; 358: 2447-2456.
104. Clifton GL, Drever P, Valadka A, Zygun D, Okonkwo D. Multicenter trial of early hypothermia in severe brain injury. J Neurotrauma 2009; 26: 393-397.
105. Clifton GL. Is keeping cool still hot? An update on hypothermia in brain injury Curr Opin Crit Care 2004; 10: 116-119.
106. Clifton GL, Valadka A, Zygun D, et al. Very early hypothermia induction in patients with severe brain injury (the National Acute Brain Injury Study: Hypothermia II): a randomised trial. Lancet Neurol 2011; 10: 131-139.
107. Kochanek PM, Safar PJ. Therapeutic hypothermia for severe traumatic brain injury. JAMA 2003; 289: 3007-3009.
108. Peterson K, Carson S, Carney N. Hypothermia treatment for traumatic brain injury: a systematic review and metaanalysis. J Neurotrauma 2008; 25: 62-71.
109. Sydenham E, Roberts I, Alderson P. Hypothermia for traumatic head injury. Cochrane Database Syst Rev 2009; CD001048.
110. Bullock MR, Povlishock JT. Guidelines for the management of severe traumatic brain injury. Editor's Commentary. J Neurotrauma 2007; 24 Suppl 1: 2 p preceding S1.
111. Bratton SL, Chestnut RM, Ghajar J, et al. Guidelines for the management of severe traumatic brain injury. III. Prophylactic hypothermia. J Neurotrauma 2007; 24 Suppl 1: S21-S25.
112. Harris OA, Muh CR, Surles MC, et al. Discrete cerebral hypothermia in the management of traumatic brain injury: a randomized controlled trial. J Neurosurg 2009; 110: 1256-1264.
113. Qiu W, Shen H, Zhang Y, et al. Noninvasive selective brain cooling by head and neck cooling is protective in severe traumatic brain injury. J Clin Neurosci 2006; 13: 995-1000.
114. Liu WG, Qiu WS, Zhang Y, Wang WM, Lu F, Yang XF. Effects of selective brain cooling in patients with severe traumatic brain injury: a preliminary study. J Int Med Res 2006; 34: 58-64.
115. Wang H, Olivero W, Lanzino G, et al. Rapid and selective cerebral hypothermia achieved using a cooling helmet. J Neurosurg 2004; 100: 272-277.
116. Shankaran S, Laptook AR, Ehrenkranz RA, et al. Wholebody hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med 2005; 353: 1574-1584.
117. Bernard SA, Gray TW, Buist MD, et al. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med 2002; 346: 557-563.
118. Hypothermia after Cardiac Arrest Study Group. Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med 2002; 346: 549-556.
119. Rouse DJ, Hirtz DG, Thom E, et al. A randomized, controlled trial of magnesium sulfate for the prevention of cerebral palsy. N Engl J Med 2008; 359: 895-905.
120. Dingley J, Tooley J, Porter H, Thoresen M. Xenon provides short-term neuroprotection in neonatal rats when administered after hypoxia-ischemia. Stroke 2006; 37: 501-506.
121. Zhu C, Kang W, Xu F, et al. Erythropoietin improved neurologic outcomes in newborns with hypoxic-ischemic encephalopathy. Pediatrics 2009; 124: e218-e226.
122. Van Bel F, Shadid M, Moison RM, et al. Effect of allopurinol on postasphyxial free radical formation, cerebral hemodynamics, and electrical brain activity. Pediatrics 1998; 101: 185-193.
123. 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.
124. Qiu WS, Liu WG, Shen H, et al. Therapeutic effect of mild hypothermia on severe traumatic head injury. Chin J Traumatol 2005; 8: 27-32.
125. Shiozaki T, Hayakata T, Taneda M, et al. A multicenter prospective randomized controlled trial of the efficacy of mild hypothermia for severely head injured patients with low intracranial pressure. Mild Hypothermia Study Group in Japan. J Neurosurg 2001; 94: 50-54.
126. Jiang J, Yu M, Zhu C. Effect of long-term mild hypothermia therapy in patients with severe traumatic brain injury: 1-year follow-up review of 87 cases. J Neurosurg 2000; 93: 546-549.