Therapeutic hypothermia for stroke: Where to go?

Experimental Neurology

Volumn 272, Issue , 2015, Pages 67-77

  Han, Ziping ^a   Liu, Xiangrong ^a   Luo, Yumin ^a,b   Ji, Xunming ^a,b  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

Author keywords

Hypothermia; Ischemic stroke; Neuroprotection

Indexed keywords

ANIMAL; COMPLICATION; HUMAN; INDUCED HYPOTHERMIA; NERVOUS SYSTEM DISEASES; PROCEDURES; STROKE;

ANIMALS; HUMANS; HYPOTHERMIA, INDUCED; NERVOUS SYSTEM DISEASES; STROKE;

EID: 84956896788     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.06.006     Document Type: Review

References (179)

1. Ahmad, M., Graham, S.H., Inflammation after stroke: mechanisms and therapeutic approaches. Transl. Stroke Res. 1 (2010), 74–84.
2. An, C., Shi, Y., Li, P., Hu, X., Gan, Y., Stetler, R.A., Leak, R.K., Gao, Y., Sun, B.L., Zheng, P., Chen, J., Molecular dialogs between the ischemic brain and the peripheral immune system: dualistic roles in injury and repair. Prog. Neurobiol. 115 (2014), 6–24.
3. Andrews, P.J., Harris, B., Murray, G.D., Randomized controlled trial of effects of the airflow through the upper respiratory tract of intubated brain-injured patients on brain temperature and selective brain cooling. Br. J. Anaesth. 94 (2005), 330–335.
4. Ao, H., Moon, J.K., Tashiro, M., Terasaki, H., Delayed platelet dysfunction in prolonged induced canine hypothermia. Resuscitation 51 (2001), 83–90.
5. Ashkenazi, A., Dixit, V.M., Death receptors: signaling and modulation. Science 281 (1998), 1305–1308.
6. Badjatia, N., Strongilis, E., Gordon, E., Prescutti, M., Fernandez, L., Fernandez, A., Buitrago, M., Schmidt, J.M., Ostapkovich, N.D., Mayer, S.A., Metabolic impact of shivering during therapeutic temperature modulation: the Bedside Shivering Assessment Scale. Stroke 39 (2008), 3242–3247.
7. Badjatia, N., Strongilis, E., Prescutti, M., Fernandez, L., Fernandez, A., Buitrago, M., Schmidt, J.M., Mayer, S.A., Metabolic benefits of surface counter warming during therapeutic temperature modulation. Crit. Care Med. 37 (2009), 1893–1897.
8. Berger, C., Schabitz, W.R., Wolf, M., Mueller, H., Sommer, C., Schwab, S., Hypothermia and brain-derived neurotrophic factor reduce glutamate synergistically in acute stroke. Exp. Neurol. 185 (2004), 305–312.
9. Bernard, S.A., Buist, M., Induced hypothermia in critical care medicine: a review. Crit. Care Med. 31 (2003), 2041–2051.
10. Bernard, S.A., Gray, T.W., Buist, M.D., Jones, B.M., Silvester, W., Gutteridge, G., Smith, K., Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N. Engl. J. Med. 346 (2002), 557–563.
11. Bi, M., Ma, Q., Zhang, S., Li, J., Zhang, Y., Lin, L., Tong, S., Wang, D., Local mild hypothermia with thrombolysis for acute ischemic stroke within a 6-h window. Clin. Neurol. Neurosurg. 113 (2011), 768–773.
12. Bristow, G.K., Sessler, D.I., Giesbrecht, G.G., Leg temperature and heat content in humans during immersion hypothermia and rewarming. Aviat. Space Environ. Med. 65 (1994), 220–226.
13. 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.
14. Ceulemans, A.G., Zgavc, T., Kooijman, R., Hachimi-Idrissi, S., Sarre, S., Michotte, Y., The dual role of the neuroinflammatory response after ischemic stroke: modulatory effects of hypothermia. J. Neuroinflammation, 7, 2010, 74.
15. Chandler, L.J., Sumners, C., Crews, F.T., Ethanol inhibits NMDA receptor-mediated excitotoxicity in rat primary neuronal cultures. Alcohol. Clin. Exp. Res. 17 (1993), 54–60.
16. Chen, J., Fredrickson, V., Ding, Y., Cheng, H., Wang, N., Ling, F., Ji, X., Enhanced neuroprotection by local intra-arterial infusion of human albumin solution and local hypothermia. Stroke 44 (2013), 260–262.
17. Chen, F., Qi, Z., Luo, Y., Hinchliffe, T., Ding, G., Xia, Y., Ji, X., Non-pharmaceutical therapies for stroke: mechanisms and clinical implications. Prog. Neurobiol. 115 (2014), 246–269.
18. Cheng, C., Matsukawa, T., Sessler, D.I., Ozaki, M., Kurz, A., Merrifield, B., Lin, H., Olofsson, P., Increasing mean skin temperature linearly reduces the core-temperature thresholds for vasoconstriction and shivering in humans. Anesthesiology 82 (1995), 1160–1168.
19. Cheng, H., Ji, X., Ding, Y., Luo, Y., Wang, G., Sun, X., Chen, J., Ling, F., Focal perfusion of circulating cooled blood reduces the infarction volume and improves neurological outcome in middle cerebral artery occlusion. Neurol. Res., 2009, 340–345.
20. Choi, J.H., Marshall, R.S., Neimark, M.A., Konstas, A.A., Lin, E., Chiang, Y.T., Mast, H., Rundek, T., Mohr, J.P., Pile-Spellman, J., Selective brain cooling with endovascular intracarotid infusion of cold saline: a pilot feasibility study. Am. J. Neuroradiol. 31 (2010), 928–934.
21. Choi, K.E., Hall, C.L., Sun, J.M., Wei, L., Mohamad, O., Dix, T.A., Yu, S.P., A novel stroke therapy of pharmacologically induced hypothermia after focal cerebral ischemia in mice. FASEB J. 26 (2012), 2799–2810.
22. Clark, D.L., Penner, M., Wowk, S., Orellana-Jordan, I., Colbourne, F., Treatments (12 and 48 h) with systemic and brain-selective hypothermia techniques after permanent focal cerebral ischemia in rat. Exp. Neurol. 220 (2009), 391–399.
23. Colbourne, F., Corbett, D., Zhao, Z., Yang, J., Buchan, A.M., Prolonged but delayed postischemic hypothermia: a long-term outcome study in the rat middle cerebral artery occlusion model. J. Cereb. Blood Flow Metab. 20 (2000), 1702–1708.
24. Corbett, D., Hamilton, M., Colbourne, F., Persistent neuroprotection with prolonged postischemic hypothermia in adult rats subjected to transient middle cerebral artery occlusion. Exp. Neurol. 163 (2000), 200–206.
25. Covaciu, L., Weis, J., Bengtsson, C., Allers, M., Lunderquist, A., Ahlstrom, H., Rubertsson, S., Brain temperature in volunteers subjected to intranasal cooling. Intensive Care Med. 37 (2011), 1277–1284.
26. Dae, M.W., Gao, D.W., Ursell, P.C., Stillson, C.A., Sessler, D.I., Safety and efficacy of endovascular cooling and rewarming for induction and reversal of hypothermia in human-sized pigs. Stroke 34 (2003), 734–738.
27. Dai, D.W., Wang, D.S., Li, K.S., Mao, Y., Zhang, L.M., Duan, S.R., Sheng, L., Effect of local mild hypothermia on expression of aquaporin-4 following intracerebral hemorrhage in rats. Zhonghua Yi Xue Za Zhi 86 (2006), 906–910.
28. De Georgia, M.A., Krieger, D.W., Abou-Chebl, A., Devlin, T.G., Jauss, M., Davis, S.M., Koroshetz, W.J., Rordorf, G., Warach, S., Cooling for Acute Ischemic Brain Damage (COOL AID): a feasibility trial of endovascular cooling. Neurology 63 (2004), 312–317.
29. De Witte, J.L., Kim, J.S., Sessler, D.I., Bastanmehr, H., Bjorksten, A.R., Tramadol reduces the sweating, vasoconstriction, and shivering thresholds. Anesth. Analg. 87 (1998), 173–179.
30. Den Hertog, H.M., van der Worp, H.B., Tseng, M.C., Dippel, D.W., Cooling therapy for acute stroke. Cochrane Database Syst. Rev., 2009, Cd001247.
31. Deng, H., Han, H.S., Cheng, D., Sun, G.H., Yenari, M.A., Mild hypothermia inhibits inflammation after experimental stroke and brain inflammation. Stroke 34 (2003), 2495–2501.
32. Deng, J., Lei, C., Chen, Y., Fang, Z., Yang, Q., Zhang, H., Cai, M., Shi, L., Dong, H., Xiong, L., Neuroprotective gases—fantasy or reality for clinical use?. Prog. Neurobiol. 115 (2014), 210–245.
33. Dietrich, W.D., Busto, R., Alonso, O., Globus, M.Y., Ginsberg, M.D., Intraischemic but not postischemic brain hypothermia protects chronically following global forebrain ischemia in rats. J. Cereb. Blood Flow Metab. 13 (1993), 541–549.
34. Ding, Y., Li, J., Rafols, J.A., Phillis, J.W., Diaz, F.G., Prereperfusion saline infusion into ischemic territory reduces inflammatory injury after transient middle cerebral artery occlusion in rats. Stroke 33 (2002), 2492–2498.
35. Ding, Y., Yao, B., Zhou, Y., Park, H., McAllister, J.P. II, Diaz, F.G., Prereperfusion flushing of ischemic territory: a therapeutic study in which histological and behavioral assessments were used to measure ischemia-reperfusion injury in rats with stroke. J. Neurosurg. 96 (2002), 310–319.
36. Ding, Y., Young, C.N., Li, J., Luan, X., McAllister, J.P. II, Clark, J.D., Diaz, F.G., Reduced inflammatory mediator expression by pre-reperfusion infusion into ischemic territory in rats: a real-time polymerase chain reaction analysis. Neurosci. Lett. 353 (2003), 173–176.
37. Ding, Y., Li, J., Luan, X., Lai, Q., McAllister, J.P. II, Phillis, J.W., Clark, J.C., Guthikonda, M., Diaz, F.G., Local saline infusion into ischemic territory induces regional brain cooling and neuroprotection in rats with transient middle cerebral artery occlusion. Neurosurgery 54 (2004), 956–964 (Discussion 964–955).
38. Dirks, M., Niessen, L.W., van Wijngaarden, J.D., Koudstaal, P.J., Franke, C.L., van Oostenbrugge, R.J., Huijsman, R., Lingsma, H.F., Minkman, M.M., Dippel, D.W., Promoting thrombolysis in acute ischemic stroke. Stroke 42 (2011), 1325–1330.
39. Donnan, G.A., Fisher, M., Macleod, M., Davis, S.M., Stroke. Lancet 371 (2008), 1612–1623.
40. Doufas, A.G., Wadhwa, A., Lin, C.M., Shah, Y.M., Hanni, K., Sessler, D.I., Neither arm nor face warming reduces the shivering threshold in unanesthetized humans. Stroke 34 (2003), 1736–1740.
41. Ehrlich, M.P., McCullough, J.N., Zhang, N., Weisz, D.J., Juvonen, T., Bodian, C.A., Griepp, R.B., Effect of hypothermia on cerebral blood flow and metabolism in the pig. Ann. Thorac. Surg. 73 (2002), 191–197.
42. Els, T., Oehm, E., Voigt, S., Klisch, J., Hetzel, A., Kassubek, J., Safety and therapeutical benefit of hemicraniectomy combined with mild hypothermia in comparison with hemicraniectomy alone in patients with malignant ischemic stroke. Cerebrovasc. Dis. 21 (2006), 79–85.
43. Emsley, H.C., Hopkins, S.J., Acute ischaemic stroke and infection: recent and emerging concepts. Lancet Neurol. 7 (2008), 341–353.
44. Esposito, E., Ebner, M., Ziemann, U., Poli, S., In cold blood: intraarteral cold infusions for selective brain cooling in stroke. J. Cereb. Blood Flow Metab. 34 (2014), 743–752.
45. Feng, J.F., Zhang, K.M., Jiang, J.Y., Gao, G.Y., Fu, X., Liang, Y.M., Effect of therapeutic mild hypothermia on the genomics of the hippocampus after moderate traumatic brain injury in rats. Neurosurgery 67 (2010), 730–742.
46. Fukuda, H., Tomimatsu, T., Watanabe, N., Mu, J.W., Kohzuki, M., Endo, M., Fujii, E., Kanzaki, T., Murata, Y., Post-ischemic hypothermia blocks caspase-3 activation in the newborn rat brain after hypoxia-ischemia. Brain Res. 910 (2001), 187–191.
47. Georgiadis, D., Schwarz, S., Kollmar, R., Schwab, S., Endovascular cooling for moderate hypothermia in patients with acute stroke: first results of a novel approach. Stroke 32 (2001), 2550–2553.
48. Georgiadis, D., Schwarz, S., Aschoff, A., Schwab, S., Hemicraniectomy and moderate hypothermia in patients with severe ischemic stroke. Stroke 33 (2002), 1584–1588.
49. Gerdeman, G., Lovinger, D.M., CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol. 85 (2001), 468–471.
50. Giraud, R., Siegenthaler, N., Bendjelid, K., Cardiac index during therapeutic hypothermia: which target value is optimal?. Crit. Care, 17, 2013, 214.
51. Globus, M.Y., Busto, R., Lin, B., Schnippering, H., Ginsberg, M.D., Detection of free radical activity during transient global ischemia and recirculation: effects of intraischemic brain temperature modulation. J. Neurochem. 65 (1995), 1250–1256.
52. Gong, P., Zhang, M.Y., Zhao, H., Tang, Z.R., Hua, R., Mei, X., Cui, J., Li, C.S., Effect of mild hypothermia on the coagulation-fibrinolysis system and physiological anticoagulants after cardiopulmonary resuscitation in a porcine model. PLoS One, 8, 2013, e67476.
53. Gonzalez-Ibarra, F.P., Varon, J., Lopez-Meza, E.G., Therapeutic hypothermia: critical review of the molecular mechanisms of action. Front. Neurol., 2, 2011, 4.
54. Green, D.R., Reed, J.C., Mitochondria and apoptosis. Science 281 (1998), 1309–1312.
55. Grigore, A.M., Grocott, H.P., Mathew, J.P., Phillips-Bute, B., Stanley, T.O., Butler, A., Landolfo, K.P., Reves, J.G., Blumenthal, J.A., Newman, M.F., The rewarming rate and increased peak temperature alter neurocognitive outcome after cardiac surgery. Anesth. Analg. 94 (2002), 4–10.
56. Gu, L.J., Xiong, X.X., Ito, T., Lee, J., Xu, B.H., Krams, S., Steinberg, G.K., Zhao, H., Moderate hypothermia inhibits brain inflammation and attenuates stroke-induced immunodepression in rats. CNS Neurosci. Ther. 20 (2014), 67–75.
57. Hacke, W., Schwab, S., Horn, M., Spranger, M., De Georgia, M., von Kummer, R., ‘Malignant’ middle cerebral artery territory infarction: clinical course and prognostic signs. Arch. Neurol. 53 (1996), 309–315.
58. Hacke, W., Kaste, M., Bluhmki, E., Brozman, M., Davalos, A., Guidetti, D., Larrue, V., Lees, K.R., Medeghri, Z., Machnig, T., Schneider, D., von Kummer, R., Wahlgren, N., Toni, D., Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N. Engl. J. Med. 359 (2008), 1317–1329.
59. Hajat, C., Hajat, S., Sharma, P., Effects of poststroke pyrexia on stroke outcome: a meta-analysis of studies in patients. Stroke 31 (2000), 410–414.
60. Hampson, A.J., Grimaldi, M., Cannabinoid receptor activation and elevated cyclic AMP reduce glutamate neurotoxicity. Eur. J. Neurosci. 13 (2001), 1529–1536.
61. Han, H.S., Qiao, Y., Karabiyikoglu, M., Giffard, R.G., Yenari, M.A., Influence of mild hypothermia on inducible nitric oxide synthase expression and reactive nitrogen production in experimental stroke and inflammation. J. Neurosci. 22 (2002), 3921–3928.
62. Han, F., Yan, S., Shi, Y., Single-prolonged stress induces endoplasmic reticulum-dependent apoptosis in the hippocampus in a rat model of post-traumatic stress disorder. PLoS One, 8, 2013, e69340.
63. Harris, B.A., Andrews, P.J., Murray, G.D., Enhanced upper respiratory tract airflow and head fanning reduce brain temperature in brain-injured, mechanically ventilated patients: a randomized, crossover, factorial trial. Br. J. Anaesth. 98 (2007), 93–99.
64. Hemmen, T.M., Raman, R., Guluma, K.Z., Meyer, B.C., Gomes, J.A., Cruz-Flores, S., Wijman, C.A., Rapp, K.S., Grotta, J.C., Lyden, P.D., Intravenous thrombolysis plus hypothermia for acute treatment of ischemic stroke (ICTuS-L): final results. Stroke 41 (2010), 2265–2270.
65. Hong, J.M., Lee, J.S., Song, H.J., Jeong, H.S., Choi, H.A., Lee, K., Therapeutic hypothermia after recanalization in patients with acute ischemic stroke. Stroke 45 (2014), 134–140.
66. Horiguchi, T., Shimizu, K., Ogino, M., Suga, S., Inamasu, J., Kawase, T., Postischemic hypothermia inhibits the generation of hydroxyl radical following transient forebrain ischemia in rats. J. Neurotrauma 20 (2003), 511–520.
67. Horstmann, S., Kalb, P., Koziol, J., Gardner, H., Wagner, S., Profiles of matrix metalloproteinases, their inhibitors, and laminin in stroke patients: influence of different therapies. Stroke 34 (2003), 2165–2170.
68. Huh, P.W., Belayev, L., Zhao, W., Koch, S., Busto, R., Ginsberg, M.D., Comparative neuroprotective efficacy of prolonged moderate intraischemic and postischemic hypothermia in focal cerebral ischemia. J. Neurosurg. 92 (2000), 91–99.
69. Imada, S., Yamamoto, M., Tanaka, K., Seiwa, C., Watanabe, K., Kamei, Y., Kozuma, S., Taketani, Y., Asou, H., Hypothermia-induced increase of oligodendrocyte precursor cells: possible involvement of plasmalemmal voltage-dependent anion channel 1. J. Neurosci. Res. 88 (2010), 3457–3466.
70. Ji, X., Luo, Y., Ling, F., Stetler, R.A., Lan, J., Cao, G., Chen, J., Mild hypothermia diminishes oxidative DNA damage and pro-death signaling events after cerebral ischemia: a mechanism for neuroprotection. Front. Biosci. 12 (2007), 1737–1747.
71. Ji, Y., Hu, Y., Wu, Y., Ji, Z., Song, W., Wang, S., Pan, S., Therapeutic time window of hypothermia is broader than cerebral artery flushing in carotid saline infusion after transient focal ischemic stroke in rats. Neurol. Res. 34 (2012), 657–663.
72. Ji, Y.B., Wu, Y.M., Ji, Z., Song, W., Xu, S.Y., Wang, Y., Pan, S.Y., Interrupted intracarotid artery cold saline infusion as an alternative method for neuroprotection after ischemic stroke. Neurosurg. Focus., 33, 2012, E10.
73. Kammersgaard, L.P., Jorgensen, H.S., Rungby, J.A., Reith, J., Nakayama, H., Weber, U.J., Houth, J., Olsen, T.S., Admission body temperature predicts long-term mortality after acute stroke: the Copenhagen Stroke Study. Stroke 33 (2002), 1759–1762.
74. Karnatovskaia, L.V., Wartenberg, K.E., Freeman, W.D., Therapeutic hypothermia for neuroprotection: history, mechanisms, risks, and clinical applications. Neurohospitalist 4 (2014), 153–163.
75. Khanna, A., Kahle, K.T., Walcott, B.P., Gerzanich, V., Simard, J.M., Disruption of ion homeostasis in the neurogliovascular unit underlies the pathogenesis of ischemic cerebral edema. Transl. Stroke Res. 5 (2014), 3–16.
76. Kim, J.Y., Kim, N., Yenari, M.A., Chang, W., Mild hypothermia suppresses calcium-sensing receptor (CaSR) induction following forebrain ischemia while increasing GABA-B receptor 1 (GABA-B-R1) expression. Transl. Stroke Res. 2 (2011), 195–201.
77. Kimberger, O., Ali, S.Z., Markstaller, M., Zmoos, S., Lauber, R., Hunkeler, C., Kurz, A., Meperidine and skin surface warming additively reduce the shivering threshold: a volunteer study. Crit. Care, 11, 2007, R29.
78. Kollmar, R., Blank, T., Han, J.L., Georgiadis, D., Schwab, S., Different degrees of hypothermia after experimental stroke: short- and long-term outcome. Stroke 38 (2007), 1585–1589.
79. Kollmar, R., Schellinger, P.D., Steigleder, T., Kohrmann, M., Schwab, S., Ice-cold saline for the induction of mild hypothermia in patients with acute ischemic stroke: a pilot study. Stroke 40 (2009), 1907–1909.
80. Krieger, D.W., Yenari, M.A., Therapeutic hypothermia for acute ischemic stroke: what do laboratory studies teach us?. Stroke 35 (2004), 1482–1489.
81. Krieger, D.W., De Georgia, M.A., Abou-Chebl, A., Andrefsky, J.C., Sila, C.A., Katzan, I.L., Mayberg, M.R., Furlan, A.J., Cooling for acute ischemic brain damage (cool aid): an open pilot study of induced hypothermia in acute ischemic stroke. Stroke 32 (2001), 1847–1854.
82. Kurasako, T., Zhao, L., Pulsinelli, W.A., Nowak, T.S. Jr., Transient cooling during early reperfusion attenuates delayed edema and infarct progression in the spontaneously hypertensive rat. Distribution and time course of regional brain temperature change in a model of postischemic hypothermic protection. J. Cereb. Blood Flow Metab. 27 (2007), 1919–1930.
83. Lai, T.W., Zhang, S., Wang, Y.T., Excitotoxicity and stroke: identifying novel targets for neuroprotection. Prog. Neurobiol. 115 (2014), 157–188.
84. Lee, S.L., Battistella, F.D., Go, K., Hypothermia induces T-cell production of immunosuppressive cytokines. J. Surg. Res. 100 (2001), 150–153.
85. Lee, J.E., Yoon, Y.J., Moseley, M.E., Yenari, M.A., Reduction in levels of matrix metalloproteinases and increased expression of tissue inhibitor of metalloproteinase-2 in response to mild hypothermia therapy in experimental stroke. J. Neurosurg. 103 (2005), 289–297.
86. Leng, T., Shi, Y., Xiong, Z.G., Sun, D., Proton-sensitive cation channels and ion exchangers in ischemic brain injury: new therapeutic targets for stroke?. Prog. Neurobiol. 115 (2014), 189–209.
87. Li, J., Luan, X., Lai, Q., Clark, J.C., McAllister, J.P. II, Fessler, R., Diaz, F.G., Ding, Y., Long-term neuroprotection induced by regional brain cooling with saline infusion into ischemic territory in rats: a behavioral analysis. Neurol. Res. 26 (2004), 677–683.
88. Li, H., Gao, A., Feng, D., Wang, Y., Zhang, L., Cui, Y., Li, B., Wang, Z., Chen, G., Evaluation of the protective potential of brain microvascular endothelial cell autophagy on blood–brain barrier integrity during experimental cerebral ischemia-reperfusion injury. Transl. Stroke Res. 5 (2014), 618–626.
89. Liu, L., Kim, J.Y., Koike, M.A., Yoon, Y.J., Tang, X.N., Ma, H., Lee, H., Steinberg, G.K., Lee, J.E., Yenari, M.A., FasL shedding is reduced by hypothermia in experimental stroke. J. Neurochem. 106 (2008), 541–550.
90. Liu, X., Wang, M., Chen, H., Guo, Y., Ma, F., Shi, F., Bi, Y., Li, Y., Hypothermia protects the brain from transient global ischemia/reperfusion by attenuating endoplasmic reticulum response-induced apoptosis through CHOP. PLoS One, 8, 2013, e53431.
91. Liu, X., Zhao, S., Liu, F., Kang, J., Xiao, A., Li, F., Zhang, C., Yan, F., Zhao, H., Luo, M., Luo, Y., Ji, X., Remote ischemic postconditioning alleviates cerebral ischemic injury by attenuating endoplasmic reticulum stress-mediated apoptosis. Transl. Stroke Res. 5 (2014), 692–700.
92. Luan, X., Li, J., McAllister, J.P. II, Diaz, F.G., Clark, J.C., Fessler, R.D., Ding, Y., Regional brain cooling induced by vascular saline infusion into ischemic territory reduces brain inflammation in stroke. Acta Neuropathol. 107 (2004), 227–234.
93. Luo, Y., Ji, X., Ling, F., Li, W., Zhang, F., Cao, G., Chen, J., Impaired DNA repair via the base-excision repair pathway after focal ischemic brain injury: a protein phosphorylation-dependent mechanism reversed by hypothermic neuroprotection. Front. Biosci. 12 (2007), 1852–1862.
94. Lyden, P.D., Allgren, R.L., Ng, K., Akins, P., Meyer, B., Al-Sanani, F., Lutsep, H., Dobak, J., Matsubara, B.S., Zivin, J., Intravascular Cooling in the Treatment of Stroke (ICTuS): early clinical experience. J. Stroke Cerebrovasc. Dis. 14 (2005), 107–114.
95. Lyden, P.D., Krieger, D., Yenari, M., Dietrich, W.D., Therapeutic hypothermia for acute stroke. Int. J. Stroke 1 (2006), 9–19.
96. Mack, W.J., Huang, J., Winfree, C., Kim, G., Oppermann, M., Dobak, J., Inderbitzen, B., Yon, S., Popilskis, S., Lasheras, J., Sciacca, R.R., Pinsky, D.J., Connolly, E.S. Jr., Ultrarapid, convection-enhanced intravascular hypothermia: a feasibility study in nonhuman primate stroke. Stroke 34 (2003), 1994–1999.
97. Macleod, M.R., Petersson, J., Norrving, B., Hacke, W., Dirnagl, U., Wagner, M., Schwab, S., Hypothermia for stroke: call to action 2010. Int. J. Stroke 5 (2010), 489–492.
98. Maier, C.M., Ahern, K., Cheng, M.L., Lee, J.E., Yenari, M.A., Steinberg, G.K., Optimal depth and duration of mild hypothermia in a focal model of transient cerebral ischemia: effects on neurologic outcome, infarct size, apoptosis, and inflammation. Stroke 29 (1998), 2171–2180.
99. Maier, C.M., Sun, G.H., Kunis, D., Yenari, M.A., Steinberg, G.K., Delayed induction and long-term effects of mild hypothermia in a focal model of transient cerebral ischemia: neurological outcome and infarct size. J. Neurosurg. 94 (2001), 90–96.
100. Maier, C.M., Sun, G.H., Cheng, D., Yenari, M.A., Chan, P.H., Steinberg, G.K., Effects of mild hypothermia on superoxide anion production, superoxide dismutase expression, and activity following transient focal cerebral ischemia. Neurobiol. Dis. 11 (2002), 28–42.
101. Martin-Schild, S., Hallevi, H., Shaltoni, H., Barreto, A.D., Gonzales, N.R., Aronowski, J., Savitz, S.I., Grotta, J.C., Combined neuroprotective modalities coupled with thrombolysis in acute ischemic stroke: a pilot study of caffeinol and mild hypothermia. J. Stroke Cerebrovasc. Dis. 18 (2009), 86–96.
102. Matsui, T., Kakeda, T., IL-10 production is reduced by hypothermia but augmented by hyperthermia in rat microglia. J. Neurotrauma 25 (2008), 709–715.
103. Matsuwaka, R., Sakakibara, T., Hori, T., Shinohara, N., Initial experience with cool head, warm body perfusion in aortic arch surgery. J. Card. Surg. 13 (1998), 463–467.
104. Mayer, S.A., Kowalski, R.G., Presciutti, M., Ostapkovich, N.D., McGann, E., Fitzsimmons, B.F., Yavagal, D.R., Du, Y.E., Naidech, A.M., Janjua, N.A., Claassen, J., Kreiter, K.T., Parra, A., Commichau, C., Clinical trial of a novel surface cooling system for fever control in neurocritical care patients. Crit. Care Med. 32 (2004), 2508–2515.
105. Meisel, C., Schwab, J.M., Prass, K., Meisel, A., Dirnagl, U., Central nervous system injury-induced immune deficiency syndrome. Nat. Rev. Neurosci. 6 (2005), 775–786.
106. Meloni, B.P., Campbell, K., Zhu, H., Knuckey, N.W., In search of clinical neuroprotection after brain ischemia: the case for mild hypothermia (35 degrees C) and magnesium. Stroke 40 (2009), 2236–2240.
107. Mirzoyev, S.A., McLeod, C.J., Bunch, T.J., Bell, M.R., White, R.D., Hypokalemia during the cooling phase of therapeutic hypothermia and its impact on arrhythmogenesis. Resuscitation 81 (2010), 1632–1636.
108. Mohr, J., Ruchholtz, S., Hildebrand, F., Flohe, S., Frink, M., Witte, I., Weuster, M., Frohlich, M., van Griensven, M., Keibl, C., Mommsen, P., Induced hypothermia does not impair coagulation system in a swine multiple trauma model. J. Trauma Acute Care Surg. 74 (2013), 1014–1020.
109. Mokhtarani, M., Mahgoub, A.N., Morioka, N., Doufas, A.G., Dae, M., Shaughnessy, T.E., Bjorksten, A.R., Sessler, D.I., Buspirone and meperidine synergistically reduce the shivering threshold. Anesth. Analg. 93 (2001), 1233–1239.
110. Mori, K., Nakao, Y., Yamamoto, T., Maeda, M., Early external decompressive craniectomy with duroplasty improves functional recovery in patients with massive hemispheric embolic infarction: timing and indication of decompressive surgery for malignant cerebral infarction. Surg. Neurol. 62 (2004), 420–429 (Discussion 429–430).
111. Morikawa, E., Ginsberg, M.D., Dietrich, W.D., Duncan, R.C., Kraydieh, S., Globus, M.Y., Busto, R., The significance of brain temperature in focal cerebral ischemia: histopathological consequences of middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 12 (1992), 380–389.
112. Mueller-Burke, D., Koehler, R.C., Martin, L.J., 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. 26 (2008), 67–76.
113. Nagel, S., Papadakis, M., Hoyte, L., Buchan, A.M., Therapeutic hypothermia in experimental models of focal and global cerebral ischemia and intracerebral hemorrhage. Expert. Rev. Neurother. 8 (2008), 1255–1268.
114. Nagel, S., Su, Y., Horstmann, S., Heiland, S., Gardner, H., Koziol, J., Martinez-Torres, F.J., Wagner, S., Minocycline and hypothermia for reperfusion injury after focal cerebral ischemia in the rat: effects on BBB breakdown and MMP expression in the acute and subacute phase. Brain Res. 1188 (2008), 198–206.
115. Nakashima, K., Todd, M.M., Effects of hypothermia on the rate of excitatory amino acid release after ischemic depolarization. Stroke 27 (1996), 913–918.
116. Nunnally, M.E., Jaeschke, R., Bellingan, G.J., Lacroix, J., Mourvillier, B., Rodriguez-Vega, G.M., Rubertsson, S., Vassilakopoulos, T., Weinert, C., Zanotti-Cavazzoni, S., Buchman, T.G., Targeted temperature management in critical care: a report and recommendations from five professional societies. Crit. Care Med. 39 (2011), 1113–1125.
117. Patel, M.D., Tilling, K., Lawrence, E., Rudd, A.G., Wolfe, C.D., McKevitt, C., Relationships between long-term stroke disability, handicap and health-related quality of life. Age Ageing 35 (2006), 273–279.
118. Perrone, S., Szabo, M., Bellieni, C.V., Longini, M., Bango, M., Kelen, D., Treszl, A., Negro, S., Tataranno, M.L., Buonocore, G., Whole body hypothermia and oxidative stress in babies with hypoxic–ischemic brain injury. Pediatr. Neurol. 43 (2010), 236–240.
119. Phanithi, P.B., Yoshida, Y., Santana, A., Su, M., Kawamura, S., Yasui, N., Mild hypothermia mitigates post-ischemic neuronal death following focal cerebral ischemia in rat brain: immunohistochemical study of Fas, caspase-3 and TUNEL. Neuropathology 20 (2000), 273–282.
120. Piehl, S., Hoefig, C.S., Scanlan, T.S., Kohrle, J., Thyronamines—past, present, and future. Endocr. Rev. 32 (2011), 64–80.
121. Piironen, K., Tiainen, M., Mustanoja, S., Kaukonen, K.M., Meretoja, A., Tatlisumak, T., Kaste, M., Mild hypothermia after intravenous thrombolysis in patients with acute stroke: a randomized controlled trial. Stroke 45 (2014), 486–491.
122. Polderman, K.H., Mechanisms of action, physiological effects, and complications of hypothermia. Crit. Care Med. 37 (2009), S186–S202.
123. Polderman, K.H., Herold, I., Therapeutic hypothermia and controlled normothermia in the intensive care unit: practical considerations, side effects, and cooling methods. Crit. Care Med. 37 (2009), 1101–1120.
124. Polderman, K.H., Rijnsburger, E.R., Peerdeman, S.M., Girbes, A.R., Induction of hypothermia in patients with various types of neurologic injury with use of large volumes of ice-cold intravenous fluid. Crit. Care Med. 33 (2005), 2744–2751.
125. Reed, S.D., Cramer, S.C., Blough, D.K., Meyer, K., Jarvik, J.G., Wang, D.Z., Treatment with tissue plasminogen activator and inpatient mortality rates for patients with ischemic stroke treated in community hospitals. Stroke 32 (2001), 1832–1840.
126. Ridenour, T.R., Warner, D.S., Todd, M.M., McAllister, A.C., Mild hypothermia reduces infarct size resulting from temporary but not permanent focal ischemia in rats. Stroke 23 (1992), 733–738.
127. Roelfsema, V., Bennet, L., George, S., Wu, D., Guan, J., Veerman, M., Gunn, A.J., Window of opportunity of cerebral hypothermia for postischemic white matter injury in the near-term fetal sheep. J. Cereb. Blood Flow Metab. 24 (2004), 877–886.
128. Rogalewski, A., Schneider, A., Ringelstein, E.B., Schabitz, W.R., Toward a multimodal neuroprotective treatment of stroke. Stroke 37 (2006), 1129–1136.
129. Rosomoff, H.L., Holaday, D.A., Cerebral blood flow and cerebral oxygen consumption during hypothermia. Am. J. Physiol. 179 (1954), 85–88.
130. Russwurm, S., Stonans, I., Schwerter, K., Stonane, E., Meissner, W., Reinhart, K., Direct influence of mild hypothermia on cytokine expression and release in cultures of human peripheral blood mononuclear cells. J. Interferon Cytokine Res. 22 (2002), 215–221.
131. Sanchez-Casado, M., Sanchez-Ledesma, M.J., Goncalves-Estella, J.M., Abad-Hernandez, M.M., Garcia-March, G., Broseta-Rodrigo, J., Effect of combination therapy with hypothermia, magnesium and tirilazad in an experimental model of diffuse cerebral ischemia. Med. Intensiva 31 (2007), 113–119.
132. Schmid-Elsaesser, R., Hungerhuber, E., Zausinger, S., Baethmann, A., Reulen, H.J., Zivin, J.A., Combination drug therapy and mild hypothermia: a promising treatment strategy for reversible, focal cerebral ischemia. Stroke 30 (1999), 1891–1899.
133. Schmidt, O.I., Heyde, C.E., Ertel, W., Stahel, P.F., Closed head injury—an inflammatory disease?. Brain Res. Rev. 48 (2005), 388–399.
134. Schmitt, K.R., Boato, F., Diestel, A., Hechler, D., Kruglov, A., Berger, F., Hendrix, S., Hypothermia-induced neurite outgrowth is mediated by tumor necrosis factor-alpha. Brain Pathol. 20 (2010), 771–779.
135. Scholler, K., Zausinger, S., Baethmann, A., Schmid-Elsaesser, R., Neuroprotection in ischemic stroke—combination drug therapy and mild hypothermia in a rat model of permanent focal cerebral ischemia. Brain Res. 1023 (2004), 272–278.
136. Schwab, S., Schwarz, S., Spranger, M., Keller, E., Bertram, M., Hacke, W., Moderate hypothermia in the treatment of patients with severe middle cerebral artery infarction. Stroke 29 (1998), 2461–2466.
137. Schwab, S., Georgiadis, D., Berrouschot, J., Schellinger, P.D., Graffagnino, C., Mayer, S.A., Feasibility and safety of moderate hypothermia after massive hemispheric infarction. Stroke 32 (2001), 2033–2035.
138. Seifert, H.A., Pennypacker, K.R., Molecular and cellular immune responses to ischemic brain injury. Transl. Stroke Res. 5 (2014), 543–553.
139. Sessler, D.I., Thermoregulatory defense mechanisms. Crit. Care Med. 37 (2009), S203–S210.
140. 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.
141. Silasi, G., Klahr, A.C., Hackett, M.J., Auriat, A.M., Nichol, H., Colbourne, F., Prolonged therapeutic hypothermia does not adversely impact neuroplasticity after global ischemia in rats. J. Cereb. Blood Flow Metab. 32 (2012), 1525–1534.
142. Song, M., Yu, S.P., Ionic regulation of cell volume changes and cell death after ischemic stroke. Transl. Stroke Res. 5 (2014), 17–27.
143. Staikou, C., Paraskeval, A., Donta, I., Theodossopoulos, T., Anastassopoulou, I., Kontos, M., The effects of mild hypothermia on coagulation tests and haemodynamic variables in anaesthetized rabbits. West Indian Med. J. 60 (2011), 513–518.
144. Stetler, R.A., Leak, R.K., Gan, Y., Li, P., Zhang, F., Hu, X., Jing, Z., Chen, J., Zigmond, M.J., Gao, Y., Preconditioning provides neuroprotection in models of CNS disease: paradigms and clinical significance. Prog. Neurobiol. 114 (2014), 58–83.
145. Taggart, R., Austin, B., Hans, E., Hogan, D., In vitro evaluation of the effect of hypothermia on coagulation in dogs via thromboelastography. J. Vet. Emerg. Crit. Care 22 (2012), 219–224.
146. Talke, P., Tayefeh, F., Sessler, D.I., Jeffrey, R., Noursalehi, M., Richardson, C., Dexmedetomidine does not alter the sweating threshold, but comparably and linearly decreases the vasoconstriction and shivering thresholds. Anesthesiology 87 (1997), 835–841.
147. Tang, X.N., Liu, L., Yenari, M.A., Combination therapy with hypothermia for treatment of cerebral ischemia. J. Neurotrauma 26 (2009), 325–331.
148. Tang, X.N., Zheng, Z., Giffard, R.G., Yenari, M.A., Significance of marrow-derived nicotinamide adenine dinucleotide phosphate oxidase in experimental ischemic stroke. Ann. Neurol. 70 (2011), 606–615.
149. Tokutomi, T., Miyagi, T., Morimoto, K., Karukaya, T., Shigemori, M., Effect of hypothermia on serum electrolyte, inflammation, coagulation, and nutritional parameters in patients with severe traumatic brain injury. Neurocrit. Care. 1 (2004), 171–182.
150. 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.
151. van der Worp, H.B., Sena, E.S., Donnan, G.A., Howells, D.W., Macleod, M.R., Hypothermia in animal models of acute ischaemic stroke: a systematic review and meta-analysis. Brain 130 (2007), 3063–3074.
152. van der Worp, H.B., Macleod, M.R., Kollmar, R., European Stroke Research Network for, H., Therapeutic hypothermia for acute ischemic stroke: ready to start large randomized trials?. J. Cereb. Blood Flow Metab. 30 (2010), 1079–1093.
153. Van Hemelrijck, A., Hachimi-Idrissi, S., Sarre, S., Ebinger, G., Michotte, Y., Neuroprotective effect of N-acetyl-aspartyl-glutamate in combination with mild hypothermia in the endothelin-1 rat model of focal cerebral ischaemia. J. Neurochem. 95 (2005), 1287–1297.
154. Wang, Y., Lim, L.L., Levi, C., Heller, R.F., Fisher, J., Influence of admission body temperature on stroke mortality. Stroke 31 (2000), 404–409.
155. Wang, Q., Li, A.L., Zhi, D.S., Huang, H.L., Effect of mild hypothermia on glucose metabolism and glycerol of brain tissue in patients with severe traumatic brain injury. Chin. J. Traumatol. 10 (2007), 246–249.
156. Wang, D., Zhao, Y., Zhang, Y., Zhang, T., Shang, X., Wang, J., Liu, Y., Kong, Q., Sun, B., Mu, L., Liu, X., Wang, G., Li, H., Hypothermia protects against oxygen-glucose deprivation-induced neuronal injury by down-regulating the reverse transport of glutamate by astrocytes as mediated by neurons. Neuroscience 237 (2013), 130–138.
157. Wartenberg, K.E., Malignant middle cerebral artery infarction. Curr. Opin. Crit. Care 18 (2012), 152–163.
158. White, B.C., Sullivan, J.M., DeGracia, D.J., O'Neil, B.J., Neumar, R.W., Grossman, L.I., Rafols, J.A., Krause, G.S., Brain ischemia and reperfusion: molecular mechanisms of neuronal injury. J. Neurol. Sci. 179 (2000), 1–33.
159. Wolberg, A.S., Meng, Z.H., Monroe, D.M. III, Hoffman, M., A systematic evaluation of the effect of temperature on coagulation enzyme activity and platelet function. J. Trauma 56 (2004), 1221–1228.
160. Wu, T.-C., Grotta, J.C., Hypothermia for acute ischaemic stroke. Lancet Neurol. 12 (2013), 275–284.
161. Xiao, F., Arnold, T.C., Zhang, S., Brown, C., Alexander, J.S., Carden, D.L., Conrad, S.A., Cerebral cortical aquaporin-4 expression in brain edema following cardiac arrest in rats. Acad. Emerg. Med. 11 (2004), 1001–1007.
162. Xie, Y.C., Li, C.Y., Li, T., Nie, D.Y., Ye, F., Effect of mild hypothermia on angiogenesis in rats with focal cerebral ischemia. Neurosci. Lett. 422 (2007), 87–90.
163. Xiong, M., Yang, Y., Chen, G.Q., Zhou, W.H., Post-ischemic hypothermia for 24 h in P7 rats rescues hippocampal neuron: association with decreased astrocyte activation and inflammatory cytokine expression. Brain Res. Bull. 79 (2009), 351–357.
164. Xiong, M., Cheng, G.Q., Ma, S.M., Yang, Y., Shao, X.M., Zhou, W.H., Post-ischemic hypothermia promotes generation of neural cells and reduces apoptosis by Bcl-2 in the striatum of neonatal rat brain. Neurochem. Int. 58 (2011), 625–633.
165. Yanamoto, H., Nagata, I., Nakahara, I., Tohnai, N., Zhang, Z., Kikuchi, H., Combination of intraischemic and postischemic hypothermia provides potent and persistent neuroprotection against temporary focal ischemia in rats. Stroke 30 (1999), 2720–2726 (discussion 2726).
166. Yenari, M.A., Han, H.S., Neuroprotective mechanisms of hypothermia in brain ischaemia. Nat. Rev. Neurosci. 13 (2012), 267–278.
167. Yenari, M.A., Han, H.S., Influence of therapeutic hypothermia on regeneration after cerebral ischemia. Front. Neurol. Neurosci. 32 (2013), 122–128.
168. Yenari, M.A., Hemmen, T.M., Therapeutic hypothermia for brain ischemia: where have we come and where do we go?. Stroke 41 (2010), S72–S74.
169. Yenari, M.A., Palmer, J.T., Bracci, P.M., Steinberg, G.K., Thrombolysis with tissue plasminogen activator (tPA) is temperature dependent. Thromb. Res. 77 (1995), 475–481.
170. Yenari, M.A., Iwayama, S., Cheng, D., Sun, G.H., Fujimura, M., Morita-Fujimura, Y., Chan, P.H., Steinberg, G.K., Mild hypothermia attenuates cytochrome c release but does not alter Bcl-2 expression or caspase activation after experimental stroke. J. Cereb. Blood Flow Metab. 22 (2002), 29–38.
171. Yenari, M., Kitagawa, K., Lyden, P., Perez-Pinzon, M., Metabolic downregulation: a key to successful neuroprotection?. Stroke 39 (2008), 2910–2917.
172. Zhang, Z., Sobel, R.A., Cheng, D., Steinberg, G.K., Yenari, M.A., Mild hypothermia increases Bcl-2 protein expression following global cerebral ischemia. Brain Res. Mol. Brain Res. 95 (2001), 75–85.
173. Zhang, F., Wang, S., Luo, Y., Ji, X., Nemoto, E.M., Chen, J., When hypothermia meets hypotension and hyperglycemia: the diverse effects of adenosine 5′-monophosphate on cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 29 (2009), 1022–1034.
174. Zhang, M., Wang, H., Zhao, J., Chen, C., Leak, R.K., Xu, Y., Vosler, P., Chen, J., Gao, Y., Zhang, F., Drug-induced hypothermia in stroke models: does it always protect?. CNS Neurol. Disord. Drug Targets 12 (2013), 371–380.
175. Zhao, H., Steinberg, G.K., Sapolsky, R.M., General versus specific actions of mild-moderate hypothermia in attenuating cerebral ischemic damage. J. Cereb. Blood Flow Metab. 27 (2007), 1879–1894.
176. Zhao, W.H., Ji, X.M., Ling, F., Ding, Y.C., Xing, C.H., Wu, H., Guo, M., Xuan, Y., Guan, B., Jiang, L.L., Local mild hypothermia induced by intra-arterial cold saline infusion prolongs the time window of onset of reperfusion injury after transient focal ischemia in rats. Neurol. Res. 31 (2009), 43–51.
177. Zhao, Q.J., Zhang, X.G., Wang, L.X., Mild hypothermia therapy reduces blood glucose and lactate and improves neurologic outcomes in patients with severe traumatic brain injury. J. Crit. Care 26 (2011), 311–315.
178. Zhou, J., Poloyac, S.M., The effect of therapeutic hypothermia on drug metabolism and response: cellular mechanisms to organ function. Expert Opin. Drug Metab. Toxicol. 7 (2011), 803–816.
179. Zweifler, R.M., Voorhees, M.E., Mahmood, M.A., Alday, D.D., Induction and maintenance of mild hypothermia by surface cooling in non-intubated subjects. J. Stroke Cerebrovasc. Dis. 12 (2003), 237–243.