Paradigms and mechanisms of inhalational anesthetics mediated neuroprotection against cerebral ischemic stroke

Medical Gas Research

Volumn 6, Issue 4, 2016, Pages 194-205

  Wang, Hailian ^a,b   Li, Peiying ^b,c   Xu, Na ^a   Zhu, Ling ^b,c   Cai, Mengfei ^a   Yu, Weifeng ^c   Gao, Yanqin ^a,b  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

inhalational anesthetics; cerebral ischemia; preconditioning; proconditioning; postconditioning; isoflurane; neuroprotection; sevoflurane

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE A1 RECEPTOR; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; AMPA RECEPTOR; CYCLOOXYGENASE 2; DESFLURANE; GELATINASE A; GELATINASE B; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3BETA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; ISOFLURANE; JANUS KINASE; LACTATE DEHYDROGENASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN BAX; PROTEIN BCL 2; SEVOFLURANE; STAT PROTEIN; TRIPHENYLTETRAZOLIUM; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1; XENON;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTIFICIAL EMBOLIZATION; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN ISCHEMIA; CARDIOPULMONARY BYPASS; CATECHOLAMINE RELEASE; CEREBRAL METABOLIC RATE OF OXYGEN; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME RELEASE; ENZYME REPRESSION; HIPPOCAMPAL CA1 REGION; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; NEUROPROTECTION; NONHUMAN; OXYGEN GLUCOSE DEPRIVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

EID: 85009288510     PISSN: None     EISSN: 20459912     Source Type: Journal    
DOI: 10.4103/2045-9912.196901     Document Type: Review

References (133)

1. Abraini JH, David HN, Lemaire M (2005) Potentially neuroprotective and therapeutic properties of nitrous oxide and xenon. Ann N Y Acad Sci1053:289-300
2. An CR, Shi YJ, Li PY, Hu XM, Gan Y, Stetler RA, Leak RK, Gao YQ, Sun BL, Zheng P, Chen J (2014) Molecular dialogs between the ischemic brain and the peripheral immune system: Dualistic roles in injury and repair. Prog Neurobiol 115:6-24
3. Aras AB, Guven M, Akman T, Ozkan A, Sen HM, Duz U, Kalkan Y, Silan C, Cosar M (2015) Neuroprotective effects of daidzein on focal cerebral ischemia injury in rats. Neural Regen Res 10:146-152
4. Arrowsmith JE, Grocott HP, Reves JG, Newman MF (2000) Central nervous system complications of cardiac surgery. Br J Anaesth 84:378-393
5. Baxter P, Chen YT, Xu Y, Swanson RA (2014) Mitochondrial dysfunction induced by nuclear poly(ADP-ribose) polymerase-1: a treatable cause of cell death in stroke. Transl Stroke Res 5:136-144
6. Beirne JP, Pearlstein RD, Massey GW, Warner DS (1998) Effect of halothane in cortical cell cultures exposed to N-methyl-D-aspartate. Neurochem Res 23:17-23
7. Bhardwaj A, Castro AF, Alkayed NJ, Hurn PD, Kirsch JR (2001) Anesthetic choice of halothane versus propofol-impact on experimental perioperative stroke. Stroke 32:1920-1925
8. Bickler PE, Fahlman CS (2004) Moderate increases in intracellular calcium activate neuroprotective signals in hippocampal neurons. Neuroscience 127:673-683
9. Bickler PE, Buck LT, Feiner JR (1995) Volatile and intravenous anesthetics decrease glutamate release from cortical brain slices during anoxia. Anesthesiology 83:1233-1240
10. Bickler PE, Zhan X, Fahlman CS (2005) Isoflurane preconditions hippocampal neurons against oxygen-glucose deprivation: role of intracellular Ca2+ and mitogen-activated protein kinase signaling. Anesthesiology 103:532-539
11. Blanck TJ, Haile M, Xu F, Zhang J, Heerdt P, Veselis RA, Beekman J, Kang R, Adamo A, Hemmings H (2000) Isoflurane pretreatment ameliorates postischemic neurologic dysfunction and preserves hippocampal Ca2+/calmodulin-dependent protein kinase in a canine cardiac arrest model. Anesthesiology 93:1285-1293
12. Bozkurt AA, Mustafa G, Tarik A, Adile O, Murat SH, Mesut K, Yildiray K, Coskun S, Murat C (2014) Syringaldehyde exerts neuroprotective effect on cerebral ischemia injury in rats through anti-oxidative and anti-apoptotic properties. Neural Regen Res 9:1884-1890
13. Breandan LS, David L, Donald MT, Christian SF, Philip EB (2002) Isoflurane prevents delayed cell death in an organotypic slice culture model of cerebral ischemia. Anesthesiology 96:189-195
14. Chen DD, Yu SP, Wei L (2014a) Ion channels in regulation of neuronal regenerative activities. Transl Stroke Res 5:156-162
15. Chen F, Qi ZF, Luo YM, Hinchliffe T, Ding GH, Xia Y, Ji XM (2014b) Non-pharmaceutical therapies for stroke: Mechanisms and clinical implications. Prog Neurobiol 115:246-269
16. David HN, Leveille F, Chazalviel L, MacKenzie ET, Buisson A, Lemaire M, Abraini JH (2003) Reduction of ischemic brain damage by nitrous oxide and xenon. J Cereb Blood Flow Metab 23:1168-1173
17. dela Pena I, Borlongan CV (2015) Translating G-CSF as an adjunct therapy to stem cell transplantation for stroke. Transl Stroke Res 6:421-429
18. Deng J, Lei C, Chen Y, Fang ZP, Yang QZ, Zhang HP, Cai M, Shi LK, Dong HL, Xiong LZ (2014) Neuroprotective gases-fantasy or reality for clinical use? Prog Neurobiol 115:210-245
19. Donnan GA, Fisher M, Macleod M, Davis SM (2008) Stroke. Lancet 371:1612-1623
20. Drummond JC, McKay LD, Cole DJ, Patel PM (2005) The role of nitric oxide synthase inhibition in the adverse effects of etomidate in the setting of focal cerebral ischemia in rats. Anesth Analg 100:841-846
21. Eilers H, Bickler PE (1996) Hypothermia and isoflurane similarly inhibit glutamate release evoked by chemical anoxia in rat cortical brain slices. Anesthesiology 85:600-607
22. Engelhard K, Werner C, Hoffman WE, Matthes B, Blobner M, Kochs E (2003) The effect of sevoflurane and propofol on cerebral neurotransmitter concentrations during cerebral ischemia in rats. Anesth Analg 97:1155-1161
23. Engelhard K, Werner C, Eberspacher E, Pape M, Blobner M, Hutzler P, Kochs E (2004) Sevoflurane and propofol influence the expression of apoptosis-regulating proteins after cerebral ischaemia and reperfusion in rats. Eur J Anaesthesiol 21:530-537
24. Fang Li Q, Xu H, Sun Y, Hu R, Jiang H (2012) Induction of inducible nitric oxide synthase by isoflurane post-conditioning via hypoxia inducible factor-1alpha during tolerance against ischemic neuronal injury. Brain Res 1451:1-9
25. Ferreira AC, Da Mesquita S, Sousa JC, Correia-Neves M, Sousa N, Palha JA, Marques F (2015) From the periphery to the brain: Lipocalin-2, a friend or foe? Prog Neurobiol 131:120-136
26. Fumagalli S, Ortolano F, De Simoni MG (2014) A close look at brain dynamics: cells and vessels seen by in vivo two-photon microscopy. Prog Neurobiol 121:36-54
27. Haelewyn B, Yvon A, Hanouz JL, MacKenzie ET, Ducouret P, Gerard JL, Roussel S (2003) Desflurane affords greater protection than halothane against focal cerebral ischaemia in the rat. Br J Anaesth 91:390-396
28. Hafez S, Hoda MN, Guo XY, Johnson MH, Fagan SC, Ergul A (2015) Comparative analysis of different methods of ischemia/ reperfusion in hyperglycemic stroke outcomes: interaction with tPA. Transl Stroke Res 6:171-180
29. Harada H, Kelly PJ, Cole DJ, Drummond JC, Patel PM (1999) Isoflurane reduces N-methyl-D-aspartate toxicity in vivo in the rat cerebral cortex. Anesth Analg 89:1442-1447
30. Harris AL, Elder J, Schiff ND, Victor JD, Goldfine AM (2014) Poststroke apathy and hypersomnia lead to worse outcomes from acute rehabilitation. Transl Stroke Res 5:292-300
31. Hill D, Coats RO, Halstead A, Burke MR (2015) A systematic research review assessing the effectiveness of pursuit interventions in spatial neglect following stroke. Transl Stroke Res 6:410-420
32. Hosaka K, Hoh BL (2014) Inflammation and cerebral aneurysms. Transl Stroke Res 5:190-198
33. Hu XM, Liou AKF, Leak RK, Xu MY, An CR, Suenaga J, Shi YJ, Gao YQ, Zheng P, Chen J (2014) Neurobiology of microglial action in CNS injuries: receptor-mediated signaling mechanisms and functional roles. Prog Neurobiol 119:60-84
34. Jungwirth B, Gordan ML, Blobner M, Schmehl W, Kochs EF, Mackensen GB (2006) Xenon impairs neurocognitive and histologic outcome after cardiopulmonary bypass combined with cerebral air embolism in rats. Anesthesiology 104:770-776
35. Kandadai MA, Meunier JM, Hart K, Holland CK, Shaw GJ (2015) Plasmin-loaded echogenic liposomes for ultrasound-mediated thrombolysis. Transl Stroke Res 6:78-87
36. Kaneko T, Yokoyama K, Makita K (2005) Late preconditioning with isoflurane in cultured rat cortical neurones. Br J Anaesth 95:662-668
37. Kapinya KJ, Lowl D, Futterer C, Maurer M, Waschke KF, Isaev NK, Dirnagl U (2002) Tolerance against ischemic neuronal injury can be induced by volatile anesthetics and is inducible NO synthase dependent. Stroke 33:1889-1898
38. Kawaguchi M, Drummond JC, Cole DJ, Kelly PJ, Spurlock MP, Patel PM (2004) Effect of isoflurane on neuronal apoptosis in rats subjected to focal cerebral ischemia. Anesth Analg 98:798-805
39. Keep RF, Wang MM, Xiang JM, Hua Y, Xi GH (2014) Full steam ahead with remote ischemic conditioning for stroke. Transl Stroke Res 5:535-537
40. Kehl F, Payne RS, Roewer N, Schurr A (2004) Sevoflurane-induced preconditioning of rat brain in vitro and the role of KATP channels. Brain Res 1021:76-81
41. Kelley RE (2001) Stroke in the postoperative period. Med Clin North Am 85:1263-1276
42. Khan MB, Hoda MN, Vaibhav K, Giri S, Wang P, Waller JL, Ergul A, Dhandapani KM, Fagan SC, Hess DC (2015) Remote ischemic postconditioning: harnessing endogenous protection in a murine model of vascular cognitive impairment. Transl Stroke Res 6:69-77
43. Khanna A, Kahle KT, Walcott BP, Gerzanich V, Simard JM (2014) Disruption of ion homeostasis in the neurogliovascular unit underlies the pathogenesis of ischemic cerebral edema. Transl Stroke Res 5:3-16
44. Kim HC, Kim E, Bae JI, Lee KH, Jeon YT, Hwang JW, Lim YJ, Min SW, Park HP (2016) Sevoflurane postconditioning reduces apoptosis by activating the JAK-STAT pathway after transient global cerebral ischemia in rats. J Neurosurg Anesthesiol 29:37-45
45. Kimbro JR, Kelly PJ, Drummond JC, Cole DJ, Patel PM (2000) Isoflurane and pentobarbital reduce AMPA toxicity in vivo in the rat cerebral cortex. Anesthesiology 92:806-812
46. Kitano H, Kirsch JR, Hurn PD, Murphy SJ (2007) Inhalational anesthetics as neuroprotectants or chemical preconditioning agents in ischemic brain. J Cereb Blood Flow Metab 27:1108-1128
47. Kudo M, Aono M, Lee Y, Massey G, Pearlstein RD, Warner DS (2001) Effects of volatile anesthetics on N-methyl-D-aspartate excitotoxicity in primary rat neuronal-glial cultures. Anesthesiology 95:756-765
48. Kurth CD, Priestley M, Watzman M, McCann J, Golden J (2001) Desflurane confers neurologic protection for deep hypothermic circulatory arrest in newborn pigs. Anesthesiology 95:959-964
49. Lai TW, Zhang S, Wang YT (2014) Excitotoxicity and stroke: Identifying novel targets for neuroprotection. Prog Neurobiol 115:157-188
50. Lapchak PA (2015) Critical early thrombolytic and endovascular reperfusion therapy for acute ischemic stroke victims: a call for adjunct neuroprotection. Transl Stroke Res 6:345-354
51. Lee JJ, Li L, Jung HH, Zuo Z (2008) Postconditioning with isoflurane reduced ischemia-induced brain injury in rats. Anesthesiology 108:1055-1062
52. Leng TD, Shi YJ, Xiong ZG, Sun DD (2014) Proton-sensitive cation channels and ion exchangers in ischemic brain injury: New therapeutic targets for stroke? Prog Neurobiol 115:189-209
53. Leung LS, Luo T, Ma JY, Herrick I (2014) Brain areas that influence general anesthesia. Prog Neurobiol 122:24-44
54. Li CX, Patel S, Wang DJ, Zhang XD (2014a) Effect of high dose isoflurane on cerebral blood flow in macaque monkeys. Magn Reson Imaging 32:956-960
55. Li G, Jia J, Fu J, Wang H, Ji K, Zang B (2014b) The effects of preconditioning and postconditioning with isoflurane on focal cerebral ischemi/reperfusion injury in rats. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue 26:431-435
56. Li HY, Gao AJ, Feng DX, Wang Y, Zhang L, Cui YH, Li B, Wang Z, Chen G (2014c) 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 5:618-626
57. Li J, Zheng S, Zuo Z (2002) I soflurane decreases AMPA-induced dark cell degeneration and edematous damage of Purkinje neurons in the rat cerebellar slices. Brain Res 958
58. Li LL, Deng J, Zuo ZY (2013) Glutamate transporter type 3 mediates isoflurane preconditioning-induced acute phase of neuroprotection in mice. Brain Res Bull 98:23-29
59. Lin D, Li G, Zuo Z (2011) Volatile anesthetic post-treatment induces protection via inhibition of glycogen synthase kinase 3beta in human neuron-like cells. Neuroscience 179:73-79
60. Liniger R, Popovic R, Sullivan B, Gregory G, Bickler PE (2001) Effects of neuroprotective cocktails on hippocampal neuron death in an in vitro model of cerebral ischemia. J Neurosurg Anesthesiol 13:19-25
61. Lioutas VA, Alfaro-Martinez F, Bedoya F, Chung CC, Pimentel DA, Novak V (2015) Intranasal insulin and insulin-like growth factor 1 as neuroprotectants in acute ischemic stroke. Transl Stroke Res 6:264-275
62. Liu JL, Wang YT, Akamatsu Y, Lee CC, Stetler RA, Lawton MT, Yang GY (2014a) Vascular remodeling after ischemic stroke: Mechanisms and therapeutic potentials. Prog Neurobiol 115:138-156
63. Liu XF, Ye RD, Yan T, Yu SP, Wei L, Xu GL, Fan XY, Jiang YJ, Stetler RA, Liu G, Chen JL (2014b) Cell based therapies for ischemic stroke: From basic science to bedside. Prog Neurobiol 115:92-115
64. Liu XR, Zhao SF, Liu F, Kang J, Xiao A, Li F, Zhang CC, Yan F, Zhao HP, Luo M, Luo YM, Ji XM (2014c) Remote ischemic postconditioning alleviates cerebral ischemic injury by attenuating endoplasmic reticulum stress-mediated apoptosis. Transl Stroke Res 5:692-700
65. Liu Y, Xiong L, Chen S, Wang Q (2006) Isoflurane tolerance against focal cerebral ischemia is attenuated by adenosine A1 receptor antagonists. Can J Anaesth 53:194-201
66. Lourenco MV, Ferreira ST, De Felice FG (2015) Neuronal stress signaling and eIF2 alpha phosphorylation as molecular links between Alzheimer's disease and diabetes. Prog Neurobiol 129:37-57
67. McBride DW, Klebe D, Tang J, Zhang JH (2015) Correcting for brain swellings effects on infarct volume calculation after middle cerebral artery occlusion in rats. Transl Stroke Res 6:323-338
68. McCully JD, Levitsky S (2003) The mitochondrial K(ATP) channel and cardioprotection. Ann Thorac Surg 75:S667-673
69. Merali Z, Leung J, Mikulis D, Silver F, Kassner A (2015) Longitudinal assessment of imatinib's effect on the blood-brain barrier after ischemia/reperfusion injury with permeability MRI. Transl Stroke Res 6:39-49
70. Ming Z, Griffith BL, Breese GR, Mueller RA, Criswell HE (2002) Changes in the effect of isoflurane on N-methyl-D-aspartic acid-gated currents in cultured cerebral cortical neurons with time in culture: evidence for subunit specificity. Anesthesiology 97:856-867
71. Miura Y, Mackensen GB, Nellgard B, Pearlstein RD, Bart RD, Dexter F, Warner DS (1999) Effects of isoflurane, ketamine, and fentanyl/ N2O on concentrations of brain and plasma catecholamines during near-complete cerebral ischemia in the rat. Anesth Analg 88:787-792
72. Nakajima Y, Moriwaki G, Ikeda K, Fujise Y (1997) The effects of sevoflurane on recovery of brain energy metabolism after cerebral ischemia in the rat: a comparison with isoflurane and halothane. Anesth Analg 85:593-599
73. Nasu I, Yokoo N, Takaoka S, Takata K, Hoshikawa T, Okada M, Miura Y (2006) The dose-dependent effects of isoflurane on outcome from severe forebrain ischemia in the rat. Anesth Analg 103:413-418
74. Nellgard B, Mackensen GB, Pineda J, Wellons JC, Pearlstein RD, Warner DS (2000) Anesthetic effects on cerebral metabolic rate predict histologic outcome from near-complete forebrain ischemia in the rat. Anesthesiology 93:431-436
75. Newberg LA, Michenfelder JD (1983) Cerebral protection by isoflurane during hypoxemia or ischemia. Anesthesiology 59:29-35
76. O'Bryant Z, Vann KT, Xiong ZG (2014) Translational strategies for neuroprotection in ischemic stroke-focusing on acid-sensing ion channel 1a. Transl Stroke Res 5:59-68
77. Obal D, Dettwiler S, Favoccia C, Scharbatke H, Preckel B, Schlack W (2005) The influence of mitochondrial KATP-channels in the cardioprotection of preconditioning and postconditioning by sevoflurane in the rat in vivo. Anesth Analg 101:1252-1260
78. Ockaili R, Emani VR, Okubo S, Brown M, Krottapalli K, Kukreja RC (1999) Opening of mitochondrial KATP channel induces early and delayed cardioprotective effect: role of nitric oxide. Am J Physiol 277:H2425-2434
79. Ohno Y, Shimizu S, Tokudome K, Kunisawa N, Sasa M (2015) New insight into the therapeutic role of the serotonergic system in Parkinson's disease. Prog Neurobiol 134:104-121
80. Peng S, Kalikiri P, Mychaskiw Ii G, Zhang D, Zhang Y, Liu GJ, Wang GL, Shen ZY (2011) Sevoflurane postconditioning ameliorates oxygen-glucose deprivation-reperfusion injury in the rat hippocampus. CNS Neurosci Ther 17:605-611
81. Petrone AB, OConnell GC, Regier MD, Chantler PD, Simpkins JW, Barr TL (2015) The role of arginase 1 in post-stroke immunosuppression and ischemic stroke severity. Transl Stroke Res 7:103-110
82. Pignataro G, Sirabella R, Anzilotti S, Di Renzo G, Annunziato L (2014) Does Na+/Ca2+ exchanger, NCX, represent a new druggable target in stroke intervention? Transl Stroke Res 5:145-155
83. Pirot S, Glowinski J, Thierry AM (1995) Excitatory responses evoked in prefrontal cortex by mediodorsal thalamic nucleus stimulation: influence of anaesthesia. Eur J Pharmacol 285:45-54
84. Raval AP, Dave KR, Mochly-Rosen D, Sick TJ, Perez-Pinzon MA (2003) Epsilon PKC is required for the induction of tolerance by ischemic and NMDA-mediated preconditioning in the organotypic hippocampal slice. J Neurosci 23:384-391
85. Reuter B, Rodemer C, Grudzenski S, Meairs S, Bugert P, Hennerici MG, Fatar M (2015) Effect of simvastatin on MMPs and TIMPs in human brain endothelial cells and experimental stroke. Transl Stroke Res 6:156-159
86. Robert P, Richard L, Philip EB (2000) Anesthetics and mild hypothermia similarly prevent hippocampal neuron death in an in vitro model of cerebral ischemia. Anesthesiology 92:1343-1349
87. Rossi D (2015) Astrocyte physiopathology: At the crossroads of intercellular networking, inflammation and cell death. Prog Neurobiol 130:86-120
88. Ruan LH, Lau BWM, Wang JX, Huang LJ, ZhuGe QC, Wang B, Jin KL, So KF (2014) Neurogenesis in neurological and psychiatric diseases and brain injury: From bench to bedside. Prog Neurobiol 115:116-137
89. Sano T, Drummond JC, Patel PM, Grafe MR, Watson JC, Cole DJ (1992) A comparison of the cerebral protective effects of isoflurane and mild hypothermia in a model of incomplete forebrain ischemia in the rat. Anesthesiology 76:221-228
90. Scheller MS, Todd MM, Drummond JC (1986) Isoflurane, halothane, and regional cerebral blood flow at various levels of PaCO2 in rabbits. Anesthesiology 64:598-604
91. Schlunzen L, Cold GE, Rasmussen M, Vafaee MS (2006) Effects of dose-dependent levels of isoflurane on cerebral blood flow in healthy subjects studied using positron emission tomography. Acta Anaesthesiol Scand 50:306-312
92. Schumacher M, Mattern C, Ghoumari A, Oudinet JP, Liere P, Labombarda F, Sitruk-Ware R, De Nicola AF, Guennoun R (2014) Revisiting the roles of progesterone and allopregnanolone in the nervous system: Resurgence of the progesterone receptors. Prog Neurobiol 113:6-39
93. Seo JH, Park HP, Jeon YT, Lim YJ, Nam K, Hwang JW (2013) Combined treatment with celecoxib and sevoflurane after global cerebral ischaemia has no additive neuroprotective effects in rats. Br J Anaesth 110:988-995
94. Shah NH, Aizenman E (2014) Voltage-gated potassium channels at the crossroads of neuronal function, ischemic tolerance, and neurodegeneration. Transl Stroke Res 5:38-58
95. Shan JH, Sun LM, Wang DW, Li XH (2015) Comparison of the neuroprotective effects and recovery profiles of isoflurane, sevoflurane and desflurane as neurosurgical pre-conditioning on ischemia/ reperfusion cerebral injury. Int J Clin Exp Pathol 8:2001-2009
96. Shenoda B (2015) The Role of Na+/Ca2+ exchanger subtypes in neuronal ischemic injury. Transl Stroke Res 6:181-190
97. Soliman S, Ishrat T, Fouda AY, Patel A, Pillai B, Fagan SC (2015) Sequential therapy with minocycline and candesartan improves long-term recovery after experimental stroke. Transl Stroke Res 6:309-322
98. Solt K, Eger EI, Raines DE (2006) Differential modulation of human N-methyl-D-aspartate receptors by structurally diverse general anesthetics. Anesth Analg 102:1407-1411
99. Song MK, Yu SP (2014) Ionic regulation of cell volume changes and cell death after ischemic stroke. Transl Stroke Res 5:17-27
100. Stetler RA, Leak RK, Gan Y, Li PY, Zhang F, Hu XM, Jing Z, Chen J, Zigmond MJ, Gao YQ (2014) Preconditioning provides neuroprotection in models of CNS disease: Paradigms and clinical significance. Prog Neurobiol 114:58-83
101. Sun M, Deng B, Zhao X, Gao C, Yang L, Zhao H, Yu D, Zhang F, Xu L, Chen L, Sun X (2015) Isoflurane preconditioning provides neuroprotection against stroke by regulating the expression of the TLR4 signalling pathway to alleviate microglial activation. Sci Rep 5:11445
102. Tanaka K, Ludwig LM, Krolikowski JG, Alcindor D, Pratt PF, Kersten JR, Pagel PS, Warltier DC (2004) Isoflurane produces delayed preconditioning against myocardial ischemia and reperfusion injury: role of cyclooxygenase-2. Anesthesiology 100:525-531
103. Thrift AG, Dewey HM, Macdonell RA, McNeil JJ, Donnan GA (2001) Incidence of the major stroke subtypes-Initial findings from the North East Melbourne Stroke Incidence Study (NEMESIS). Stroke 32:1732-1738
104. Toner CC, Milne AJ, Blatchford KL, McLaughlin DP, Stamford JA (2002) An assessment of the cerebroprotective potential of volatile anaesthetics using two independent methods in an in vitro model of cerebral ischaemia. Brain Res 958:390-398
105. Toner CC, Connelly K, Whelpton R, Bains S, Michael-Titus AT, McLaughlin DP, Stamford JA (2001) Effects of sevoflurane on dopamine, glutamate and aspartate release in an in vitro model of cerebral ischaemia. Br J Anaesth 86:550-554
106. Tong L, Wu Z, Ran M, Chen Y, Yang L, Zhang H, Zhang L, Dong H, Xiong L (2015) The role of sumo-conjugating enzyme Ubc9 in the neuroprotection of isoflurane preconditioning against ischemic neuronal injury. Mol Neurobiol 51:1221-1231
107. Tsai SK, Lin SM, Hung WC, Mok MS, Chih CL, Huang SS (2004) The effect of desflurane on ameliorating cerebral infarction in rats subjected to focal cerebral ischemia-reperfusion injury. Life Sci 74:2541-2549
108. Vargas-Martinez F, Uvnas-Moberg K, Petersson M, Olausson HA, Jimenez-Estrada I (2014) Neuropeptides as neuroprotective agents: oxytocin a forefront developmental player in the mammalian brain. Prog Neurobiol 123:37-78
109. Verhaegen MJ, Todd MM, Warner DS (1992) A comparison of cerebral ischemic flow thresholds during halothane N2O and isoflurane N2O anesthesia in rats. Anesthesiology 76:743-754
110. Waje-Andreassen U, Naess H, Thomassen L, Maroy TH, Mazengia KY, Eide GE, Vedeler CA (2015) Biomarkers related to carotid intima-media thickness and plaques in long-term survivors of ischemic stroke. Transl Stroke Res 6:276-283
111. Wang C, Jin Lee J, Jung HH, Zuo Z (2007a) Pretreatment with volatile anesthetics, but not with the nonimmobilizer 1,2-dichlorohexafluorocyclobutane, reduced cell injury in rat cerebellar slices after an in vitro simulated ischemia. Brain Res 1152:201-208
112. Wang H, Lu S, Yu Q, Liang W, Gao H, Li P, Gan Y, Chen J, Gao Y (2011) Sevoflurane preconditioning confers neuroprotection via anti-inflammatory effects. Front Biosci (Elite Ed)3:604-615
113. Wang HL, Shi H, Yu Q, Chen J, Zhang F, Gao YQ (2016) Sevoflurane preconditioning confers neuroprotection via anti-apoptosis effects. Acta Neurochir Suppl 121:55-61
114. Wang J, Lei B, Popp S, Meng F, Cottrell JE, Kass IS (2007b) Sevoflurane immediate preconditioning alters hypoxic membrane potential changes in rat hippocampal slices and improves recovery of CA1 pyramidal cells after hypoxia and global cerebral ischemia. Neuroscience 145:1097-1107
115. Wang L, Wang X, Su H, Han Z, Yu H, Wang D, Jiang R, Liu Z, Zhang J (2015) Recombinant human erythropoietin improves the neurofunctional recovery of rats following traumatic brain injury via an increase in circulating endothelial progenitor cells. Transl Stroke Res 6:50-59
116. Warner DS (2004) Anesthetics provide limited but real protection against acute brain injury. J Neurosurg Anesthesiol 16:303-307
117. Waterford SD, Rastegar M, Goodwin E, Lapchak PA, Juan V, Haji F, Bombien R, Khoynezhad A (2015) Methodology of motor evoked potentials in a rabbit model. Transl Stroke Res 6:399-406
118. Wen XR, Fu YY, Liu HZ, Wu J, Shao XP, Zhang XB, Tang M, Shi Y, Ma K, Zhang F, Wang YW, Tang H, Han D, Zhang P, Wang SL, Xu Z, Song YJ (2016) Neuroprotection of sevoflurane against ischemia/reperfusion-induced brain injury through inhibiting JNK3/Caspase-3 by enhancing Akt signaling pathway. Mol Neurobiol 53:1661-1671
119. Wise-Faberowski L, Raizada MK, Sumners C (2001) Oxygen and glucose deprivation-induced neuronal apoptosis is attenuated by halothane and isoflurane. Anesth Analg 93:1281-1287
120. Wu L, Zhao H, Wang T, Pac-Soo C, Ma D (2014) Cellular signaling pathways and molecular mechanisms involving inhalational anesthetics-induced organoprotection. J Anesth 28:740-758
121. Xiong LZ, Zheng Y, Wu MC, Hou LC, Zhu ZH, Zhang XJ, Lu ZH (2003) Preconditioning with isoflurane produces dose-dependent neuroprotection via activation of adenosine triphosphate-regulated potassium channels after focal cerebral ischemia in rats. Anesth Analg 96:233-237
122. Yan YY, Wang XM, Jiang Y, Chen H, He JT, Mang J, Shao YK, Xu ZX (2015) The role of Rho/Rho-kinase pathway and the neuroprotective effects of fasudil in chronic cerebral ischemia. Neural Regen Res 10:1441-1449
123. Yu B, Zhou SL, Yi S, Gu XS (2015) The regulatory roles of noncoding RNAs in nerve injury and regeneration. Prog Neurobiol 134:122-139
124. Yu Q, Chu M, Wang H, Lu S, Gao H, Li P, Gan Y, Shi H, Liang W, Chen J, Gao Y (2011) Sevoflurane preconditioning protects blood-brain-barrier against brain ischemia. Front Biosci (Elite Ed) 3:978-988
125. Zausinger S, Baethmann A, Schmid-Elsaesser R (2002) Anesthetic methods in rats determine outcome after experimental focal cerebral ischemia: mechanical ventilation is required to obtain controlled experimental conditions. Brain Res Protocols 9:112-121
126. Zheng M, Du H, Ni W, Koch LG, Britton SL, Keep RF, Xi G, Hua Y (2015) Iron-induced necrotic brain cell death in rats with different aerobic capacity. Transl Stroke Res 6:215-223
127. Zheng SQ, Zuo ZY (2003) Isoflurane preconditioning reduces purkinje cell death in an in vitro model of rat cerebellar ischemia. Neuroscience 118:99-106
128. Zheng SQ, Zuo ZY (2004) Isoflurane preconditioning induces neuroprotection against ischemia via activation of P38 mitogen-activated protein kinases. Mol Pharmacol 65:1172-1180
129. Zheng SQ, Zuo ZY (2005) Isoflurane preconditioning decreases glutamate receptor overactivation-induced Purkinje neuronal injury in rat cerebellar slices. Brain Res 1054:143-151
130. Zhou Y, Wang YC, Wang J, Stetler RA, Yang QW (2014) Inflammation in intracerebral hemorrhage: From mechanisms to clinical translation. Prog Neurobiol 115:25-44
131. Zhu H, Zhang Y, Shi Z, Lu D, Li T, Ding Y, Ruan Y, Xu A (2016) The Neuroprotection of liraglutide against ischaemia-induced apoptosis through the activation of the PI3K/AKT and MAPK pathways. Sci Rep 6:26859
132. Zhu W, Casper A, Libal NL, Murphy SJ, Bodhankar S, Offner H, Alkayed NJ (2014) Preclinical evaluation of recombinant t cell receptor ligand RTL1000 as a therapeutic agent in ischemic stroke. Transl Stroke Res 6:60-68
133. Zhu W, Wang L, Zhang L, Palmateer JM, Libal NL, Hurn PD, Herson PS, Murphy SJ (2010) Isoflurane preconditioning neuroprotection in experimental focal stroke is androgen-dependent in male mice. Neuroscience 169:758-769