Therapeutic hypothermia and targeted temperature management in traumatic brain injury: Clinical challenges for successful translation

Brain Research

Volumn 1640, Issue , 2016, Pages 94-103

  Dietrich, W Dalton ^a   Bramlett, Helen M ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Clinical; Experimental; Hypothermia; Secondary injury mechanisms; Temperature management

Indexed keywords

BRAIN TEMPERATURE; CLINICAL STUDY; EXPERIMENTAL TRAUMATIC BRAIN INJURY; HUMAN; HYPOTHERMIA; INDUCED HYPOTHERMIA; NONHUMAN; OUTCOME ASSESSMENT; PRECLINICAL STUDY; PRIORITY JOURNAL; REVIEW; TEMPERATURE SENSITIVITY; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURIES, TRAUMATIC; CLINICAL TRIAL (TOPIC); PATHOPHYSIOLOGY; PROCEDURES;

ANIMALS; BRAIN INJURIES, TRAUMATIC; CLINICAL TRIALS AS TOPIC; HUMANS; HYPOTHERMIA, INDUCED;

EID: 84953776332     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.12.034     Document Type: Review

References (115)

1. (POLAR-RCT), (POLAR-RCT), T.P.H.T.t.L.T.B.I. Vol., ed.^eds. ClinicalTrials.gov Identifier: NCT00987688.
2. Adelson, P.D., Wisniewski, S.R., Beca, J., Brown, S.D., Bell, M., Muizelaar, J.P., Okada, P., Beers, S.R., Balasubramani, G.K., Hirtz, D., Paediatric Traumatic Brain Injury, C., Comparison of hypothermia and normothermia after severe traumatic brain injury in children (Cool Kids): a phase 3, randomised controlled trial. Lancet Neurol. 12 (2013), 546–553.
3. Alzaga, A.G., Salazar, G.A., Varon, J., Resuscitation great. Breaking the thermal barrier: Dr. Temple Fay. Resuscitation 69 (2006), 359–364.
4. Andrews, P.J., Sinclair, H.L., Battison, C.G., Polderman, K.H., Citerio, G., Mascia, L., Harris, B.A., Murray, G.D., Stocchetti, N., Menon, D.K., Shakur, H., De Backer, D., EurothermTrial, c, European society of intensive care medicine study of therapeutic hypothermia (32-35 degrees C) for intracranial pressure reduction after traumatic brain injury (the Eurotherm3235Trial). Trials, 12, 2011, 8.
5. Andrews, P.J., Sinclair, H.L., Rodriguez, A., Harris, B.A., Battison, C.G., Rhodes, J.K., Murray, G.D., Eurotherm Trial, C., Hypothermia for intracranial hypertension after traumatic brain Injury. N Engl. J. Med, 2015.
6. Atkins, C.M., Oliva, A.A. Jr., Alonso, O.F., Chen, S., Bramlett, H.M., Hu, B.R., Dietrich, W.D., Hypothermia treatment potentiates ERK1/2 activation after traumatic brain injury. Eur. J. Neurosci. 26 (2007), 810–819.
7. Atkins, C.M., Truettner, J.S., Lotocki, G., Sanchez-Molano, J., Kang, Y., Alonso, O.F., Sick, T.J., Dietrich, W.D., Bramlett, H.M., Post-traumatic seizure susceptibility is attenuated by hypothermia therapy. Eur. J. Neurosci. 32 (2010), 1912–1920.
8. Bao, L., Chen, D., Ding, L., Ling, W., Xu, F., Fever burden is an independent predictor for prognosis of traumatic brain injury. PLoS One, 9, 2014, e90956.
9. Beca, J., McSharry, B., Erickson, S., Yung, M., Schibler, A., Slater, A., Wilkins, B., Singhal, A., Williams, G., Sherring, C., Butt, W., Pediatric Study Group of the, A., New Zealand Intensive Care Society Clinical Trials, G., Hypothermia for traumatic brain injury in children-A Phase II randomized controlled trial. Crit. Care Med. 43 (2015), 1458–1466.
10. Brain Trauma, F., American Association of Neurological, S., Congress of Neurological, S., Guidelines for the management of severe traumatic brain injury. J. Neurotrauma. 24:Suppl. 1 (2007), S1–S106.
11. Bramlett, H., Dietrich, W.D. 3rd, Long-term consequences of traumatic brain injury: current status of potential mechanisms of injury and neurologic outcomes. J. Neurotrauma, 2014.
12. Bramlett, H.M., Green, E.J., Dietrich, W.D., Busto, R., Globus, M.Y., Ginsberg, M.D., Posttraumatic brain hypothermia provides protection from sensorimotor and cognitive behavioral deficits. J. Neurotrauma 12 (1995), 289–298.
13. Bramlett, H.M., Dietrich, W.D., Green, E.J., Busto, R., Chronic histopathological consequences of fluid-percussion brain injury in rats: effects of post-traumatic hypothermia. Acta Neuropathol. 93 (1997), 190–199.
14. Bramlett, H.M., Dietrich, W.D., The effects of posttraumatic hypothermia on diffuse axonal injury following parasaggital fluid percussion brain injury in rats. Ther. Hypothermia Temp. Manag. 2 (2012), 14–23.
15. Bregy, A., Nixon, R., Lotocki, G., Alonso, O.F., Atkins, C.M., Tsoulfas, P., Bramlett, H.M., Dietrich, W.D., Posttraumatic hypothermia increases doublecortin expressing neurons in the dentate gyrus after traumatic brain injury in the rat. Exp. Neurol. 233 (2012), 821–828.
16. Busto, R., Dietrich, W.D., Globus, M.Y., Valdes, I., Scheinberg, P., Ginsberg, M.D., Small differences in intraischemic brain temperature critically determine the extent of ischemic neuronal injury. J. Cereb. Blood Flow Metab. 7 (1987), 729–738.
17. Chase, A., Traumatic brain injury. No benefit of progesterone therapy in patients with TBI. Nat. Rev. Neurol., 11, 2015, 65.
18. Chatzipanteli, K., Wada, K., Busto, R., Dietrich, W.D., Effects of moderate hypothermia on constitutive and inducible nitric oxide synthase activities after traumatic brain injury in the rat. J. Neurochem. 72 (1999), 2047–2052.
19. Chatzipanteli, K., Alonso, O.F., Kraydieh, S., Dietrich, W.D., Importance of posttraumatic hypothermia and hyperthermia on the inflammatory response after fluid percussion brain injury: biochemical and immunocytochemical studies. J. Cereb. Blood Flow Metab. 20 (2000), 531–542.
20. Chesnut, R.M., Marshall, L.F., Klauber, M.R., Blunt, B.A., Baldwin, N., Eisenberg, H.M., Jane, J.A., Marmarou, A., Foulkes, M.A., The role of secondary brain injury in determining outcome from severe head injury. J. Trauma. 34 (1993), 216–222.
21. Chesnut, R.M., Marshall, S.B., Piek, J., Blunt, B.A., Klauber, M.R., Marshall, L.F., Early and late systemic hypotension as a frequent and fundamental source of cerebral ischemia following severe brain injury in the Traumatic Coma Data Bank. Acta Neurochir. Suppl. (Wien.) 59 (1993), 121–125.
22. Clifton, G.L., Jiang, J.Y., Lyeth, B.G., Jenkins, L.W., Hamm, R.J., Hayes, R.L., Marked protection by moderate hypothermia after experimental traumatic brain injury. J. Cereb. Blood Flow Metab. 11 (1991), 114–121.
23. Clifton, G.L., Choi, S.C., Miller, E.R., Levin, H.S., Smith, K.R. Jr., Muizelaar, J.P., Wagner, F.C. Jr., Marion, D.W., Luerssen, T.G., Intercenter variance in clinical trials of head trauma--experience of the National Acute Brain Injury Study: Hypothermia. J. Neurosurg. 95 (2001), 751–755.
24. Clifton, G.L., Miller, E.R., Choi, S.C., Levin, H.S., McCauley, S., Smith, K.R. Jr., Muizelaar, J.P., Wagner, F.C. Jr., Marion, D.W., Luerssen, T.G., Chesnut, R.M., Schwartz, M., Lack of effect of induction of hypothermia after acute brain injury. N. Engl. J. Med. 344 (2001), 556–563.
25. Clifton, G.L., Valadka, A., Zygun, D., Coffey, C.S., Drever, P., Fourwinds, S., Janis, L.S., Wilde, E., Taylor, P., Harshman, K., Conley, A., Puccio, A., Levin, H.S., McCauley, S.R., Bucholz, R.D., Smith, K.R., Schmidt, J.H., Scott, J.N., Yonas, H., Okonkwo, D.O., Very early hypothermia induction in patients with severe brain injury (the National Acute Brain Injury Study: Hypothermia II): a randomised trial. Lancet Neurol. 10 (2011), 131–139.
26. Corrigan, J.D., Selassie, A.W., Orman, J.A., The epidemiology of traumatic brain injury. J. Head Trauma Rehabil. 25 (2010), 72–80.
27. Crossley, S., Reid, J., McLatchie, R., Hayton, J., Clark, C., MacDougall, M., Andrews, P.J., A systematic review of therapeutic hypothermia for adult patients following traumatic brain injury. Crit. Care, 18, 2014, R75.
28. Dietrich, W.D., The importance of brain temperature in cerebral injury. J. Neurotrauma. 9:Suppl. 2 (1992), S475–S485.
29. Dietrich, W.D., Alonso, O., Busto, R., Globus, M.Y., Ginsberg, M.D., Post-traumatic brain hypothermia reduces histopathological damage following concussive brain injury in the rat. Acta Neuropathol. 87 (1994), 250–258.
30. Dietrich, W.D., Alonso, O., Halley, M., Busto, R., Delayed posttraumatic brain hyperthermia worsens outcome after fluid percussion brain injury: a light and electron microscopic study in rats. Neurosurgery 38 (1996), 533–541 discussion 541.
31. Dietrich, W.D., Bramlett, H.M., Hyperthermia and central nervous system injury. Prog. Brain Res. 162 (2007), 201–217.
32. Dietrich, W.D., Atkins, C.M., Bramlett, H.M., Protection in animal models of brain and spinal cord injury with mild to moderate hypothermia. J. Neurotrauma 26 (2009), 301–312.
33. Dietrich, W.D., Bramlett, H.M., The evidence for hypothermia as a neuroprotectant in traumatic brain injury. Neurotherapeutics 7 (2010), 43–50.
34. Diringer, M.N., Neurocritical Care Fever Reduction Trial, G., Treatment of fever in the neurologic intensive care unit with a catheter-based heat exchange system. Crit. Care Med. 32 (2004), 559–564.
35. Dixon, C.E., Markgraf, C.G., Angileri, F., Pike, B.R., Wolfson, B., Newcomb, J.K., Bismar, M.M., Blanco, A.J., Clifton, G.L., Hayes, R.L., Protective effects of moderate hypothermia on behavioral deficits but not necrotic cavitation following cortical impact injury in the rat. J. Neurotrauma 15 (1998), 95–103.
36. Faul, M.X.L., Wald, M.M., Coronado, V.G., Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations, and Deaths. Vol., Centers for Disease Control and Prevention. 2010, National Center for Injury Prevention and Control, Atlanta, GA.
37. Fay, T., Observations on generalized refrigeration in cases of severe cerebral trauma. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 4 (1945), 611–619.
38. Finkelstein, E.A., Corso, P.S., Miller, T.R., The Incidence and Economic Burden of Injuries in the United States. Vol, 2006, Oxford University Press, New York.
39. Flynn, L.M., Rhodes, J., Andrews, P.J., Therapeutic Hypothermia Reduces Intracranial Pressure and Partial Brain Oxygen Tension in Patients with Severe Traumatic Brain Injury: Preliminary Data from the Eurotherm3235 Trial. Ther. Hypothermia Temp. Manag. 5 (2015), 143–151.
40. Gaither, J.B., Galson, S., Curry, M., Mhayamaguru, M., Williams, C., Keim, S.M., Bobrow, B.J., Spaite, D.W., Environmental Hyperthermia in Prehospital Patients with Major Traumatic Brain Injury. J. Emerg. Med. 49 (2015), 375–381.
41. Globus, M.Y., Alonso, O., Dietrich, W.D., Busto, R., Ginsberg, M.D., Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia. J. Neurochem. 65 (1995), 1704–1711.
42. Gu, X., Wei, Z.Z., Espinera, A., Lee, J.H., Ji, X., Wei, L., Dix, T.A., Yu, S.P., Pharmacologically induced hypothermia attenuates traumatic brain injury in neonatal rats. Exp. Neurol. 267 (2015), 135–142.
43. Han, Z., Liu, X., Luo, Y., Ji, X., 2015. Therapeutic hypothermia for stroke: where to go?. Exp. Neurol 272 (2014), 67–77.
44. Hifumi, T., Kuroda, Y., Kawakita, K., Yamashita, S., Oda, Y., Dohi, K., Maekawa, T., Fever control management is preferable to mild therapeutic hypothermia in traumatic brain injury patients with abbreviated injury scale 3-4: a multi-center, randomized controlled trial. J. Neurotrauma, 2015 [Epub ahead of print].
45. Howard, R.B., Sayeed, I., Stein, D., Suboptimal dosing parameters as possible factors in the negative Phase III clinical trials of progesterone in TBI. J. Neurotrauma., 2015 [Epub ahead of print].
46. Hutchison, J.S., Ward, R.E., Lacroix, J., Hebert, P.C., Barnes, M.A., Bohn, D.J., Dirks, P.B., Doucette, S., Fergusson, D., Gottesman, R., Joffe, A.R., Kirpalani, H.M., Meyer, P.G., Morris, K.P., Moher, D., Singh, R.N., Skippen, P.W., Hypothermia Pediatric Head Injury Trial, I., the Canadian Critical Care Trials, G., Hypothermia therapy after traumatic brain injury in children. N. Engl. J. Med. 358 (2008), 2447–2456.
47. Jiang, J.Y., Lyeth, B.G., Kapasi, M.Z., Jenkins, L.W., Povlishock, J.T., Moderate hypothermia reduces blood-brain barrier disruption following traumatic brain injury in the rat. Acta Neuropathol. 84 (1992), 495–500.
48. Jin, Y., Lin, Y., Feng, J.F., Jia, F., Gao, G., Jiang, J.Y., Attenuation of cell death in injured cortex after post-traumatic brain injury moderate hypothermia: possible involvement of autophagy pathway. World Neurosurg. 84 (2015), 420–430.
49. Karnatovskaia, L.V., Wartenberg, K.E., Freeman, W.D., Therapeutic hypothermia for neuroprotection: history, mechanisms, risks, and clinical applications. Neurohospitalist 4 (2014), 153–163.
50. Kilpatrick, M.M., Lowry, D.W., Firlik, A.D., Yonas, H., Marion, D.W., Hyperthermia in the neurosurgical intensive care unit. Neurosurgery 47:850-5 (2000), 855–856.
51. Kinoshita, K., Chatzipanteli i, K., Vitarbo, E., Truettner, J.S., Alonso, O.F., Dietrich, W.D., Interleukin-1beta messenger ribonucleic acid and protein levels after fluid-percussion brain injury in rats: importance of injury severity and brain temperature. Neurosurgery 51 (2002), 195–203 discussion 203.
52. Kinoshita, K., Chatzipanteli, K., Alonso, O.F., Howard, M., Dietrich, W.D., The effect of brain temperature on hemoglobin extravasation after traumatic brain injury. J. Neurosurg. 97 (2002), 945–953.
53. Kochanek, P.M., Jackson, T.C., It might be time to let cooler heads prevail after mild traumatic brain injury or concussion. Exp. Neurol. 267 (2015), 13–17.
54. Langlois, J.A., Rutland-Brown, W., Wald, M.M., The epidemiology and impact of traumatic brain injury: a brief overview. J. Head. Trauma Rehabil. 21 (2006), 375–378.
55. Lei, J., Gao, G., Mao, Q., Feng, J., Wang, L., You, W., Jiang, J., collaborators, L.T.Ht, Rationale, methodology, and implementation of a nationwide multicenter randomized controlled trial of long-term mild hypothermia for severe traumatic brain injury (the LTH-1 trial). Contemp. Clin. Trials 40 (2015), 9–14.
56. Leonov, Y., Sterz, F., Safar, P., Radovsky, A., Oku, K., Tisherman, S., Stezoski, S.W., Mild cerebral hypothermia during and after cardiac arrest improves neurologic outcome in dogs. J. Cereb. Blood Flow Metab. 10 (1990), 57–70.
57. Li, J., Jiang, J.Y., Chinese Head Trauma Data Bank: effect of hyperthermia on the outcome of acute head trauma patients. J. Neurotrauma. 29 (2012), 96–100.
58. Li, P., Yang, C., Moderate hypothermia treatment in adult patients with severe traumatic brain injury: a meta-analysis. Brain Inj. 28 (2014), 1036–1041.
59. Li, Y.H., Zhang, C.L., Zhang, X.Y., Zhou, H.X., Meng, L.L., Effects of mild induced hypothermia on hippocampal connexin 43 and glutamate transporter 1 expression following traumatic brain injury in rats. Mol. Med. Rep. 11 (2015), 1991–1996.
60. Lotocki, G., de Rivero Vaccari, J.P., Perez, E.R., Sanchez-Molano, J., Furones-Alonso, O., Bramlett, H.M., Dietrich, W.D., Alterations in blood-brain barrier permeability to large and small molecules and leukocyte accumulation after traumatic brain injury: effects of post-traumatic hypothermia. J. Neurotrauma. 26 (2009), 1123–1134.
61. Lotocki, G., de Rivero Vaccari, J.P., Alonso, O., Molano, J.S., Nixon, R., Safavi, P., Dietrich, W.D., Bramlett, H.M., Oligodendrocyte vulnerability following traumatic brain injury in rats. Neurosci. Lett. 499 (2011), 143–148.
62. Lyeth, B.G., Jiang, J.Y., Liu, S., Behavioral protection by moderate hypothermia initiated after experimental traumatic brain injury. J. Neurotrauma 10 (1993), 57–64.
63. Ma, M., Matthews, B.T., Lampe, J.W., Meaney, D.F., Shofer, F.S., Neumar, R.W., Immediate short-duration hypothermia provides long-term protection in an in vivo model of traumatic axonal injury. Exp. Neurol. 215 (2009), 119–127.
64. Madden, L.K., DeVon, H.A., A Systematic Review of the Effects of Body Temperature on Outcome After Adult Traumatic Brain Injury. J. Neurosci. Nurs. 47 (2015), 190–203.
65. Maekawa, T., 2015. Therapeutic Hypothermia for Severe Traumatic Brain Injury in Japan. Vol., ed.^eds.
66. Maekawa, T., Yamashita, S., Nagao, S., Hayashi, N., Ohashi, Y., Brain-Hypothermia Study, G., Prolonged mild therapeutic hypothermia versus fever control with tight hemodynamic monitoring and slow rewarming in patients with severe traumatic brain injury: a randomized controlled trial. J. Neurotrauma 32 (2015), 422–429.
67. Marion, D., Bullock, M.R., Current and future role of therapeutic hypothermia. J. Neurotrauma 26 (2009), 455–467.
68. Marion, D.W., Penrod, L.E., Kelsey, S.F., Obrist, W.D., Kochanek, P.M., Palmer, A.M., Wisniewski, S.R., DeKosky, S.T., Treatment of traumatic brain injury with moderate hypothermia. N Engl. J. Med. 336 (1997), 540–546.
69. Marion, D.W., Regasa, L.E., Revisiting therapeutic hypothermia for severe traumatic brain injur. again. Crit. Care, 18, 2014, 160.
70. Markgraf, C.G., Clifton, G.L., Moody, M.R., Treatment window for hypothermia in brain injury. J. Neurosurg. 95 (2001), 979–983.
71. Marklund, N., Hillered, L., Animal modelling of traumatic brain injury in preclinical drug development: where do we go from here?. Br. J. Pharmacol. 164 (2011), 1207–1229.
72. Matsushita, Y., Bramlett, H.M., Alonso, O., Dietrich, W.D., Posttraumatic hypothermia is neuroprotective in a model of traumatic brain injury complicated by a secondary hypoxic insult. Crit. Care Med. 29 (2001), 2060–2066.
73. Natale, J.E., Joseph, J.G., Helfaer, M.A., Shaffner, D.H., Early hyperthermia after traumatic brain injury in children: risk factors, influence on length of stay, and effect on short-term neurologic status. Crit. Care Med. 28 (2000), 2608–2615.
74. Newmyer, R., Mendelson, J., Pang, D., Fink, E.L., Targeted temperature management in pediatric central nervous system disease. Curr. Treat. Options Pediatr. 1 (2015), 38–47.
75. Nichol, A., Gantner, D., Presneill, J., Murray, L., Trapani, T., Bernard, S., Cameron, P., Capellier, G., Forbes, A., McArthur, C., Newby, L., Rashford, S., Rosenfeld, J.V., Smith, T., Stephenson, M., Varma, D., Walker, T., Webb, S., Cooper, D.J., Protocol for a multicentre randomised controlled trial of early and sustained prophylactic hypothermia in the management of traumatic brain injury. Crit. Care Resusc. 17 (2015), 92–100.
76. Nielsen, N., Wetterslev, J., Cronberg, T., Erlinge, D., Gasche, Y., Hassager, C., Horn, J., Hovdenes, J., Kjaergaard, J., Kuiper, M., Pellis, T., Stammet, P., Wanscher, M., Wise, M.P., Aneman, A., Al-Subaie, N., Boesgaard, S., Bro-Jeppesen, J., Brunetti, I., Bugge, J.F., Hingston, C.D., Juffermans, N.P., Koopmans, M., Kober, L., Langorgen, J., Lilja, G., Moller, J.E., Rundgren, M., Rylander, C., Smid, O., Werer, C., Winkel, P., Friberg, H., Investigators, T.T.M.T., Targeted temperature management at 33 degrees C versus 36 degrees C after cardiac arrest. N. Engl. J. Med. 369 (2013), 2197–2206.
77. Polderman, K.H., Tjong Tjin Joe, R., Peerdeman, S.M., Vandertop, W.P., Girbes, A.R., Effects of therapeutic hypothermia on intracranial pressure and outcome in patients with severe head injury. Intensive Care Med. 28 (2002), 1563–1573.
78. Polderman, K.H., Application of therapeutic hypothermia in the ICU: opportunities and pitfalls of a promising treatment modality. Part 1: Indications and evidence. Intensive Care Med. 30 (2004), 556–575.
79. Polderman, K.H., Mayer, S.A., Menon, D., Hypothermia therapy after traumatic brain injury in children. N Engl. J. Med., 359, 2008, 1178 author reply 1180.
80. Polderman, K.H., Mechanisms of action, physiological effects, and complications of hypothermia. Crit. Care Med. 37 (2009), S186–S202.
81. Polderman, K.H., Andrews, P.J., Hypothermia in patients with brain injury: the way forward?. Lancet Neurol. 10:404-5 (2011), 406–407.
82. Povlishock, J.T., Wei, E.P., Posthypothermic rewarming considerations following traumatic brain injury. J. Neurotrauma. 26 (2009), 333–340.
83. Radosevich, J.J., Patanwala, A.E., Erstad, B.L., Emerging pharmacological agents to improve survival from traumatic brain injury. Brain Inj. 27 (2013), 1492–1499.
84. Rincon, F., Hunter, K., Schorr, C., Dellinger, R.P., Zanotti-Cavazzoni, S., The epidemiology of spontaneous fever and hypothermia on admission of brain injury patients to intensive care units: a multicenter cohort study. J. Neurosurg. 121 (2014), 950–960.
85. Robertson, C.S., Valadka, A.B., Hannay, H.J., Contant, C.F., Gopinath, S.P., Cormio, M., Uzura, M., Grossman, R.G., Prevention of secondary ischemic insults after severe head injury. Crit. Care Med. 27 (1999), 2086–2095.
86. Robertson, C.S., Hannay, H.J., Yamal, J.M., Gopinath, S., Goodman, J.C., Tilley, B.C., Epo Severe, T.B.I.T.I., Baldwin, A., Rivera Lara, L., Saucedo-Crespo, H., Ahmed, O., Sadasivan, S., Ponce, L., Cruz-Navarro, J., Shahin, H., Aisiku, I.P., Doshi, P., Valadka, A., Neipert, L., Waguspack, J.M., Rubin, M.L., Benoit, J.S., Swank, P., Effect of erythropoietin and transfusion threshold on neurological recovery after traumatic brain injury: a randomized clinical trial. JAMA 312 (2014), 36–47.
87. Robertson, C.S., Ropper, A.H., Getting warmer on critical care for head injury. N. Engl. J. Med, 2015.
88. Rosomoff, H.L., Holaday, D.A., Cerebral blood flow and cerebral oxygen consumption during hypothermia. Am. J. Physiol. 179 (1954), 85–88.
89. Rosomoff, H.L., Safar, P., Management of the comatose patient. Clin. Anesth. 1 (1965), 244–258.
90. Sadaka, F., Veremakis, C., Therapeutic hypothermia for the management of intracranial hypertension in severe traumatic brain injury: a systematic review. Brain Inj. 26 (2012), 899–908.
91. Safar, P., Resuscitation from clinical death: pathophysiologic limits and therapeutic potentials. Crit. Care Med. 16 (1988), 923–941.
92. Sakurai, A., Atkins, C.M., Alonso, O.F., Bramlett, H.M., Dietrich, W.D., Mild hyperthermia worsens the neuropathological damage associated with mild traumatic brain injury in rats. J. Neurotrauma. 29 (2012), 313–321.
93. Schreckinger, M., Marion, D.W., Contemporary management of traumatic intracranial hypertension: is there a role for therapeutic hypothermia?. Neurocritical Care. 11 (2009), 427–436.
94. Shiozaki, T., Sugimoto, H., Taneda, M., Yoshida, H., Iwai, A., Yoshioka, T., Sugimoto, T., Effect of mild hypothermia on uncontrollable intracranial hypertension after severe head injury. J. Neurosurg. 79 (1993), 363–368.
95. Silasi, G., Colbourne, F., Therapeutic hypothermia influences cell genesis and survival in the rat hippocampus following global ischemia. J. Cereb. Blood Flow Metab. 31 (2011), 1725–1735.
96. Skolnick, B.E., Maas, A.I., Narayan, R.K., van der Hoop, R.G., MacAllister, T., Ward, J.D., Nelson, N.R., Stocchetti, N., Investigators, S.T., A clinical trial of progesterone for severe traumatic brain injury. N. Engl. J. Med. 371 (2014), 2467–2476.
97. Smith, S.L., Hall, E.D., Mild pre- and posttraumatic hypothermia attenuates blood-brain barrier damage following controlled cortical impact injury in the rat. J. Neurotrauma 13 (1996), 1–9.
98. Suehiro, E., Koizumi, H., Fujisawa, H., Fujita, M., Kaneko, T., Oda, Y., Yamashita, S., Tsuruta, R., Maekawa, T., Suzuki, M., Diverse effects of hypothermia therapy in patients with severe traumatic brain injury based on the computed tomography classification of the traumatic coma data bank. J. Neurotrauma. 32 (2015), 353–358.
99. Suzuki, T., Bramlett, H.M., Dietrich, W.D., The importance of gender on the beneficial effects of posttraumatic hypothermia. Exp. Neurol. 184 (2003), 1017–1026.
100. Suzuki, T., Bramlett, H.M., Ruenes, G., Dietrich, W.D., The effects of early post-traumatic hyperthermia in female and ovariectomized rats. J. Neurotrauma. 21 (2004), 842–853.
101. Thompson, H.J., Pinto-Martin, J., Bullock, M.R., Neurogenic fever after traumatic brain injury: an epidemiological study. J. Neurol. Neurosurg. Psychiatry 74 (2003), 614–619.
102. Thurman, D.J., Alverson, C., Dunn, K.A., Guerrero, J., Sniezek, J.E., Traumatic brain injury in the United States: A public health perspective. J. Head Trauma Rehabil. 14 (1999), 602–615.
103. Titus, D.J., Furones, C., Atkins, C.M., Dietrich, W.D., Emergence of cognitive deficits after mild traumatic brain injury due to hyperthermia. Exp. Neurol. 263 (2015), 254–262.
104. Todd, M.M., Hindman, B.J., Clarke, W.R., Torner, J.C., Weeks, J.B., Bayman, E.O., Shi, Q., Spofford, C.M., Investigators, I., Perioperative fever and outcome in surgical patients with aneurysmal subarachnoid hemorrhage. Neurosurgery 64 (2009), 897–908 discussion 908.
105. Truettner, J.S., Suzuki, T., Dietrich, W.D., The effect of therapeutic hypothermia on the expression of inflammatory response genes following moderate traumatic brain injury in the rat. Brain Res. Mol. Brain Res. 138 (2005), 124–134.
106. Vitarbo, E.A., Chatzipanteli, K., Kinoshita, K., Truettner, J.S., Alonso, O.F., Dietrich, W.D., Tumor necrosis factor alpha expression and protein levels after fluid percussion injury in rats: the effect of injury severity and brain temperature. Neurosurgery 55:416-24 (2004), 424–425.
107. Wang, H., Olivero, W., Wang, D., Lanzino, G., Cold as a therapeutic agent. Acta Neurochir. 148:565-70 (2006), 569–570.
108. Wright, D.W., Yeatts, S.D., Silbergleit, R., Palesch, Y.Y., Hertzberg, V.S., Frankel, M., Goldstein, F.C., Caveney, A.F., Howlett-Smith, H., Bengelink, E.M., Manley, G.T., Merck, L.H., Janis, L.S., Barsan, W.G., Investigators, N., Very early administration of progesterone for acute traumatic brain injury. N. Engl. J. Med. 371 (2014), 2457–2466.
109. Yenari, M.A., Han, H.S., Neuroprotective mechanisms of hypothermia in brain ischaemia. Nat. Rev. Neurosci. 13 (2012), 267–278.
110. Yenari, M.A., Han, H.S., Influence of therapeutic hypothermia on regeneration after cerebral ischemia. Front. Neurol. Neurosci. 32 (2013), 122–128.
111. Yokobori, S., Frantzen, J., Bullock, R., Gajavelli, S., Burks, S., Bramlett, H., Dietrich, W.D., The use of hypothermia therapy in traumatic ischemic/reperfusional brain injury: review of the literatures. Ther. Hypothermia Temp. Manag. 1 (2011), 185–192.
112. Yokobori, S., Bullock, R., Gajavelli, S., Burks, S., Mondello, S., Mo, J., Wang, K.K., Hayes, R.L., Bramlett, H., Dietrich, D., Preoperative-induced mild hypothermia attenuates neuronal damage in a rat subdural hematoma model. Acta Neurochir. Suppl. 118 (2013), 77–81.
113. Yokobori, S., Gajavelli, S., Mondello, S., Mo-Seaney, J., Bramlett, H.M., Dietrich, W.D., Bullock, M.R., Neuroprotective effect of preoperatively induced mild hypothermia as determined by biomarkers and histopathological estimation in a rat subdural hematoma decompression model. J. Neurosurg. 118 (2013), 370–380.
114. Yu, C.G., Jagid, J., Ruenes, G., Dietrich, W.D., Marcillo, A.E., Yezierski, R.P., Detrimental effects of systemic hyperthermia on locomotor function and histopathological outcome after traumatic spinal cord injury in the rat. Neurosurgery 49:152-8 (2001), 158–159.
115. Zhang, B.F., Wang, J., Liu, Z.W., Zhao, Y.L., Li, D.D., Huang, T.Q., Gu, H., Song, J.N., Meta-analysis of the efficacy and safety of therapeutic hypothermia in children with acute traumatic brain injury. World Neurosurg. 83 (2015), 567–573.