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Preconditioning and protection against ischaemia–reperfusion in non-cardiac organs: a place for volatile anaesthetics?

Published online by Cambridge University Press:  01 September 2007

G. Minguet ,
J. Joris  and
M. Lamy
G. Minguet*
Affiliation:
University of Liège, Department of Anaesthesia and Intensive Care Medicine, Belgium
J. Joris
Affiliation:
University of Liège, Department of Anaesthesia and Intensive Care Medicine, Belgium
M. Lamy
Affiliation:
University of Liège, Department of Anaesthesia and Intensive Care Medicine, Belgium
*
Correspondence to: Grégory Minguet, Department of Anaesthesia and Intensive Care Medicine, CHU de Liège, B35 Domaine Universitaire du Sart Tilman, B-4000 Liège 1, Belgium. E-mail: gminguet@chu.ulg.ac.be; Tel: +32 4 366 71 79; Fax: +32 4 366 76 36
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Summary

There is an increasing body of evidence that volatile anaesthetics protect myocardium against ischaemic insult by a mechanism termed ‘anaesthetic preconditioning’. Anaesthetic preconditioning and ischaemic preconditioning share several common mechanisms of action. Since ischaemic preconditioning has been demonstrated in organs other than the heart, anaesthetic preconditioning might also apply in these organs and have significant clinical applications in surgical procedures carrying a high risk of ischaemia–reperfusion injury. After a brief review on myocardial preconditioning, experimental and clinical data on preconditioning in non-cardiac tissues will be presented. Potential benefits of anaesthetic preconditioning during non-cardiac surgery will be addressed.

Keywords

ANAESTHESIA: ANAESTHETICS INHALATIONISCHAEMIA–REPERFUSIONMITOCHONDRIAISCHAEMIC PRECONDITIONING
Type
Review
Information
European Journal of Anaesthesiology , Volume 24 , Issue 9 , September 2007 , pp. 733 - 745
Copyright
Copyright © European Society of Anaesthesiology 2007

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References

1.Murry, CE, Jennings, RB, Reimer, KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74: 1124–1136.CrossRefGoogle ScholarPubMed
2.Yellon, DM, Downey, JM. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 2003; 83: 1113–1151.CrossRefGoogle ScholarPubMed
3.Zaugg, M, Lucchinetti, E, Uecker, M, Pasch, T, Schaub, MC. Anaesthetics and cardiac preconditioning. Part I. Signalling and cytoprotective mechanisms. Br J Anaesth 2003; 91: 551–565.CrossRefGoogle ScholarPubMed
4.Yamashita, N, Hoshida, S, Taniguchi, N, Kuzuya, T, Hori, M. Whole-body hyperthermia provides biphasic cardioprotection against ischemia/reperfusion injury in the rat. Circulation 1998; 98: 1414–1421.CrossRefGoogle ScholarPubMed
5.Ovize, M, Kloner, RA, Przyklenk, K. Stretch preconditions canine myocardium. Am J Physiol 1994; 266: H137–H146.Google ScholarPubMed
6.Koning, MM, Gho, BC, van Klaarwater, E et al. . Rapid ventricular pacing produces myocardial protection by nonischemic activation of K(ATP) channels. Circulation 1996; 93: 178–186.CrossRefGoogle Scholar
7.Parratt, JR, Vegh, A, Kaszala, K, Papp, JG. Protection by preconditioning and cardiac pacing against ventricular arrhythmias resulting from ischemia and reperfusion. Ann NY Acad Sci 1996; 793: 98–107.CrossRefGoogle ScholarPubMed
8.Tritto, I, D'Andrea, D, Eramo, N et al. . Oxygen radicals can induce preconditioning in rabbit hearts. Circ Res 1997; 80: 743–748.CrossRefGoogle ScholarPubMed
9.Miyawaki, H, Zhou, X, Ashraf, M. Calcium preconditioning elicits strong protection against ischemic injury via protein kinase C signaling pathway. Circ Res 1996; 79: 137–146.CrossRefGoogle ScholarPubMed
10.Lynch, C. Anesthetic preconditioning: not just for the heart? Anesthesiology 1999; 91: 606–608.CrossRefGoogle Scholar
11.Cason, BA, Gamperl, AK, Slocum, RE, Hickey, RF. Anesthetic-induced preconditioning: previous administration of isoflurane decreases myocardial infarct size in rabbits. Anesthesiology 1997; 87: 1182–1190.CrossRefGoogle ScholarPubMed
12.Kersten, JR, Schmeling, TJ, Pagel, PS, Gross, GJ, Warltier, DC. Isoflurane mimics ischemic preconditioning via activation of K(ATP) channels: reduction of myocardial infarct size with an acute memory phase. Anesthesiology 1997; 87: 361–370.CrossRefGoogle ScholarPubMed
13.De Hert, SG, Turani, F, Mathur, S, Stowe, DF. Cardioprotection with volatile anesthetics: mechanisms and clinical implications. Anesth Analg 2005; 100: 1584–1593.CrossRefGoogle ScholarPubMed
14.Symons, JA, Myles, PS. Myocardial protection with volatile anaesthetic agents during coronary artery bypass surgery: a meta-analysis. Br J Anaesth 2006; 97: 127–136.CrossRefGoogle ScholarPubMed
15.Carroll, R, Gant, VA, Yellon, DM. Mitochondrial K(ATP) channel opening protects a human atrial-derived cell line by a mechanism involving free radical generation. Cardiovasc Res 2001; 51: 691–700.CrossRefGoogle ScholarPubMed
16.Krenz, M, Oldenburg, O, Wimpee, H et al. . Opening of ATP-sensitive potassium channels causes generation of free radicals in vascular smooth muscle cells. Basic Res Cardiol 2002; 97: 365–373.CrossRefGoogle ScholarPubMed
17.Riess, ML, Camara, AK, Novalija, E et al. . Anesthetic preconditioning attenuates mitochondrial Ca2+ overload during ischemia in guinea pig intact hearts: reversal by 5-hydroxydecanoic acid. Anesth Analg 2002; 95: 1540–1546, table of contents.CrossRefGoogle ScholarPubMed
18.Piriou, V, Chiari, P, Gateau-Roesch, O et al. . Desflurane-induced preconditioning alters calcium-induced mitochondrial permeability transition. Anesthesiology 2004; 100: 581–588.CrossRefGoogle ScholarPubMed
19.Riess, ML, Novalija, E, Camara, AK et al. . Preconditioning with sevoflurane reduces changes in nicotinamide adenine dinucleotide during ischemia–reperfusion in isolated hearts: reversal by 5-hydroxydecanoic acid. Anesthesiology 2003; 98: 387–395.CrossRefGoogle ScholarPubMed
20.Novalija, E, Kevin, LG, Eells, JT, Henry, MM, Stowe, DF. Anesthetic preconditioning improves adenosine triphosphate synthesis and reduces reactive oxygen species formation in mitochondria after ischemia by a redox dependent mechanism. Anesthesiology 2003; 98: 1155–1163.CrossRefGoogle ScholarPubMed
21.Bolli, R. The late phase of preconditioning. Circ Res 2000; 87: 972–983.CrossRefGoogle ScholarPubMed
22.Shi, Y, Hutchins, WC, Su, J et al. . Delayed cardioprotection with isoflurane: role of reactive oxygen and nitrogen. Am J Physiol Heart Circ Physiol 2005; 288: H175–H184.CrossRefGoogle ScholarPubMed
23.Sergeev, P, da Silva, R, Lucchinetti, E et al. . Trigger-dependent gene expression profiles in cardiac preconditioning: evidence for distinct genetic programs in ischemic and anesthetic preconditioning. Anesthesiology 2004; 100: 474–488.CrossRefGoogle ScholarPubMed
24.Tanaka, K, Ludwig, LM, Krolikowski, JG et al. . Isoflurane produces delayed preconditioning against myocardial ischemia and reperfusion injury: role of cyclooxygenase-2. Anesthesiology 2004; 100: 525–531.CrossRefGoogle ScholarPubMed
25.Tonkovic-Capin, M, Gross, GJ, Bosnjak, ZJ et al. . Delayed cardioprotection by isoflurane: role of K(ATP) channels. Am J Physiol Heart Circ Physiol 2002; 283: H61–H68.CrossRefGoogle ScholarPubMed
26.Richard, V, Kaeffer, N, Tron, C, Thuillez, C. Ischemic preconditioning protects against coronary endothelial dysfunction induced by ischemia and reperfusion. Circulation 1994; 89: 1254–1261.CrossRefGoogle ScholarPubMed
27.Kaeffer, N, Richard, V, Francois, A et al. . Preconditioning prevents chronic reperfusion-induced coronary endothelial dysfunction in rats. Am J Physiol 1996; 271: H842–H849.Google ScholarPubMed
28.Rubino, A, Yellon, DM. Ischaemic preconditioning of the vasculature: an overlooked phenomenon for protecting the heart? Trends Pharmacol Sci 2000; 21: 225–230.CrossRefGoogle ScholarPubMed
29.Headrick, JP, Hack, B, Ashton, KJ. Acute adenosinergic cardioprotection in ischemic-reperfused hearts. Am J Physiol Heart Circ Physiol 2003; 285: H1797–H1818.CrossRefGoogle ScholarPubMed
30.Hata, K, Whittaker, P, Kloner, RA, Przyklenk, K. Brief antecedent ischemia attenuates platelet-mediated thrombosis in damaged and stenotic canine coronary arteries: role of adenosine. Circulation 1998; 97: 692–702.CrossRefGoogle ScholarPubMed
31.DeFily, DV, Chilian, WM. Preconditioning protects coronary arteriolar endothelium from ischemia–reperfusion injury. Am J Physiol 1993; 265: H700–H706.Google ScholarPubMed
32.Liu, R, Ishibe, Y, Ueda, M, Hang, Y. Isoflurane administration before ischemia and during reperfusion attenuates ischemia/reperfusion-induced injury of isolated rabbit lungs. Anesth Analg 1999; 89: 561–565.CrossRefGoogle ScholarPubMed
33.Kaul, TK, Fields, BL, Riggins, LS et al. . Adult respiratory distress syndrome following cardiopulmonary bypass: incidence, prophylaxis and management. J Cardiovasc Surg (Torino) 1998; 39: 777–781.Google ScholarPubMed
34.de Perrot, M, Liu, M, Waddell, TK, Keshavjee, S. Ischemia–reperfusion-induced lung injury. Am J Respir Crit Care Med 2003; 167: 490–511.CrossRefGoogle ScholarPubMed
35.Tang, DG, Pavot, DR, Mouria, MM, Holwitt, DM, Cohen, NM. Warm ischemia lung protection with pinacidil: an ATP regulated potassium channel opener. Ann Thorac Surg 2003; 76: 385–389, iscussion 389–390.CrossRefGoogle ScholarPubMed
36.Waldow, T, Alexiou, K, Witt, W et al. . Protection of lung tissue against ischemia/reperfusion injury by preconditioning with inhaled nitric oxide in an in situ pig model of normothermic pulmonary ischemia. Nitric Oxide 2004; 10: 195–201.CrossRefGoogle Scholar
37.Obal, D, Dettwiler, S, Favoccia, C et al. . Effect of sevoflurane preconditioning on ischaemia/reperfusion injury in the rat kidney in vivo. Eur J Anaesthesiol 2006; 23: 319–326.CrossRefGoogle ScholarPubMed
38.Hashiguchi, H, Morooka, H, Miyoshi, H et al. . Isoflurane protects renal function against ischemia and reperfusion through inhibition of protein kinases, JNK and ERK. Anesth Analg 2005; 101: 1584–1589.CrossRefGoogle ScholarPubMed
39.Lee, HT, Ota-Setlik, A, Fu, Y, Nasr, SH, Emala, CW. Differential protective effects of volatile anesthetics against renal ischemia–reperfusion injury in vivo. Anesthesiology 2004; 101: 1313–1324.CrossRefGoogle ScholarPubMed
40.Zager, RA, Iwata, M, Burkhart, KM, Schimpf, BA. Post-ischemic acute renal failure protects proximal tubules from O2 deprivation injury, possibly by inducing uremia. Kidney Int 1994; 45: 1760–1768.CrossRefGoogle ScholarPubMed
41.Zager, RA, Burkhart, KM, Gmur, DJ. Postischemic proximal tubular resistance to oxidant stress and Ca2+ ionophore-induced attack. Implications for reperfusion injury. Lab Invest 1995; 72: 592–600.Google ScholarPubMed
42.Bonventre, JV. Kidney ischemic preconditioning. Curr Opin Nephrol Hypertens 2002; 11: 43–48.CrossRefGoogle ScholarPubMed
43.Heemann, U, Szabo, A, Hamar, P et al. . Lipopolysaccharide pretreatment protects from renal ischemia/reperfusion injury: possible connection to an interleukin-6-dependent pathway. Am J Pathol 2000; 156: 287–293.CrossRefGoogle Scholar
44.Redaelli, CA, Tien, YH, Kubulus, D et al. . Hyperthermia preconditioning induces renal heat shock protein expression, improves cold ischemia tolerance, kidney graft function and survival in rats. Nephron 2002; 90: 489–497.CrossRefGoogle ScholarPubMed
45.Lee, HT, Emala, CW. Protective effects of renal ischemic preconditioning and adenosine pretreatment: role of A(1) and A(3) receptors. Am J Physiol Renal Physiol 2000; 278: F380–F387.CrossRefGoogle Scholar
46.Okusa, MD, Linden, J, Huang, L et al. . A(2a) adenosine receptor-mediated inhibition of renal injury and neutrophil adhesion. Am J Physiol Renal Physiol 2000; 279: F809–F818.CrossRefGoogle ScholarPubMed
47.Yang, CW, Ahn, HJ, Han, HJ et al. . Pharmacological preconditioning with low-dose cyclosporine or FK506 reduces subsequent ischemia/reperfusion injury in rat kidney. Transplantation 2001; 72: 1753–1759.CrossRefGoogle ScholarPubMed
48.Bellomo, R, Bonventre, J, Macias, W, Pinsky, M. Management of early acute renal failure: focus on post-injury prevention. Curr Opin Crit Care 2005; 11: 542–547.CrossRefGoogle ScholarPubMed
49.Imai, M, Kon, S, Inaba, H. Effects of halothane, isoflurane and sevoflurane on ischemia–reperfusion injury in the perfused liver of fasted rats. Acta Anaesthesiol Scand 1996; 40: 1242–1248.CrossRefGoogle ScholarPubMed
50.Jassem, W, Fuggle, SV, Cerundolo, L, Heaton, ND, Rela, M. Ischemic preconditioning of cadaver donor livers protects allografts following transplantation. Transplantation 2006; 81: 169–174.CrossRefGoogle ScholarPubMed
51.Clavien, PA, Selzner, M, Rudiger, HA et al. . A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg 2003; 238: 843–850.CrossRefGoogle ScholarPubMed
52.Rudiger, HA, Kang, KJ, Sindram, D, Riehle, HM, Clavien, PA. Comparison of ischemic preconditioning and intermittent and continuous inflow occlusion in the murine liver. Ann Surg 2002; 235: 400–407.CrossRefGoogle ScholarPubMed
53.Clavien, PA, Yadav, S, Sindram, D, Bentley, RC. Protective effects of ischemic preconditioning for liver resection performed under inflow occlusion in humans. Ann Surg 2000; 232: 155–162.CrossRefGoogle ScholarPubMed
54.Chouker, A, Schachtner, T, Schauer, R et al. . Effects of pringle manoeuvre and ischaemic preconditioning on haemodynamic stability in patients undergoing elective hepatectomy: a randomized trial. Br J Anaesth 2004; 93: 204–211.CrossRefGoogle ScholarPubMed
55.Selzner, N, Rudiger, H, Graf, R, Clavien, PA. Protective strategies against ischemic injury of the liver. Gastroenterology 2003; 125: 917–936.CrossRefGoogle ScholarPubMed
56.Rensing, H, Bauer, I, Kubulus, D et al. . Heme oxygenase-1 gene expression in pericentral hepatocytes through beta1-adrenoceptor stimulation. Shock 2004; 21: 376–387.CrossRefGoogle ScholarPubMed
57.Ito, K, Ozasa, H, Sanada, K, Horikawa, S. Doxorubicin preconditioning: a protection against rat hepatic ischemia–reperfusion injury. Hepatology 2000; 31: 416–419.CrossRefGoogle ScholarPubMed
58.Mallick, IH, Yang, W, Winslet, MC, Seifalian, AM. Ischemia–reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 2004; 49: 1359–1377.CrossRefGoogle ScholarPubMed
59.Collard, CD, Gelman, S. Pathophysiology, clinical manifestations, and prevention of ischemia–reperfusion injury. Anesthesiology 2001; 94: 1133–1138.CrossRefGoogle ScholarPubMed
60.Hotter, G, Closa, D, Prados, M et al. . Intestinal preconditioning is mediated by a transient increase in nitric oxide. Biochem Biophys Res Commun 1996; 222: 27–32.CrossRefGoogle ScholarPubMed
61.Sola, A, De Oca, J, Gonzalez, R et al. . Protective effect of ischemic preconditioning on cold preservation and reperfusion injury associated with rat intestinal transplantation. Ann Surg 2001; 234: 98–106.CrossRefGoogle ScholarPubMed
62.Wang, SF, Li, GW. Early protective effect of ischemic preconditioning on small intestinal graft in rats. World J Gastroenterol 2003; 9: 1866–1870.CrossRefGoogle ScholarPubMed
63.Aksoyek, S, Cinel, I, Avlan, D et al. . Intestinal ischemic preconditioning protects the intestine and reduces bacterial translocation. Shock 2002; 18: 476–480.CrossRefGoogle ScholarPubMed
64.Tamion, F, Richard, V, Lacoume, Y, Thuillez, C. Intestinal preconditioning prevents systemic inflammatory response in hemorrhagic shock. Role of HO-1. Am J Physiol Gastrointest Liver Physiol 2002; 283: G408–G414.CrossRefGoogle ScholarPubMed
65.Thomas, S, Pulimood, A, Balasubramanian, KA. Heat preconditioning prevents oxidative stress-induced damage in the intestine and lung following surgical manipulation. Br J Surg 2003; 90: 473–481.CrossRefGoogle ScholarPubMed
66.Zhang, Y, Wu, YX, Hao, YB, Dun, Y, Yang, SP. Role of endogenous opioid peptides in protection of ischemic preconditioning in rat small intestine. Life Sci 2001; 68: 1013–1019.CrossRefGoogle ScholarPubMed
67.Zheng, S, Zuo, Z. Isoflurane preconditioning induces neuroprotection against ischemia via activation of p38 mitogen-activated protein kinases. Mol Pharmacol 2004; 65: 1172–1180.CrossRefGoogle ScholarPubMed
68.Kitagawa, K, Matsumoto, M, Tagaya, M et al. . ‘Ischemic tolerance’ phenomenon found in the brain. Brain Res 1990; 528: 21–24.CrossRefGoogle ScholarPubMed
69.Kirino, T. Ischemic tolerance. J Cereb Blood Flow Metab 2002; 22: 1283–1296.CrossRefGoogle ScholarPubMed
70.Sitzer, M, Foerch, C, Neumann-Haefelin, T et al. . Transient ischaemic attack preceding anterior circulation infarction is independently associated with favourable outcome. J Neurol Neurosurg Psychiatry 2004; 75: 659–660.CrossRefGoogle ScholarPubMed
71.Gidday, JM, Fitzgibbons, JC, Shah, AR, Park, TS. Neuroprotection from ischemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci Lett 1994; 168: 221–224.CrossRefGoogle ScholarPubMed
72.Ikeda, T, Xia, XY, Xia, YX, Ikenoue, T. Hyperthermic preconditioning prevents blood-brain barrier disruption produced by hypoxia–ischemia in newborn rat. Brain Res Dev Brain Res 1999; 117: 53–58.CrossRefGoogle ScholarPubMed
73.Toyoda, T, Kassell, NF, Lee, KS. Induction of tolerance against ischemia/reperfusion injury in the rat brain by preconditioning with the endotoxin analog diphosphoryl lipid a. J Neurosurg 2000; 92: 435–441.CrossRefGoogle ScholarPubMed
74.Shimizu, K, Lacza, Z, Rajapakse, N et al. . Mito K(ATP) opener, diazoxide, reduces neuronal damage after middle cerebral artery occlusion in the rat. Am J Physiol Heart Circ Physiol 2002; 283: H1005–H1011.CrossRefGoogle Scholar
75.Sirin, BH, Ortac, R, Cerrahoglu, M et al. . Ischaemic preconditioning reduces spinal cord injury in transient ischaemia. Acta Cardiol 2002; 57: 279–285.CrossRefGoogle ScholarPubMed
76.Toumpoulis, IK, Anagnostopoulos, CE, Drossos, GE et al. . Early ischemic preconditioning without hypotension prevents spinal cord injury caused by descending thoracic aortic occlusion. J Thorac Cardiovasc Surg 2003; 125: 1030–1036.CrossRefGoogle ScholarPubMed
77.Caparrelli, DJ, IICattaneo, SM, Bethea, BT et al. . Pharmacological preconditioning ameliorates neurological injury in a model of spinal cord ischemia. Ann Thorac Surg 2002; 74: 838–844.CrossRefGoogle Scholar
78.Zhang, P, Abraham, VS, Kraft, KR et al. . Hyperthermic preconditioning protects against spinal cord ischemic injury. Ann Thorac Surg 2000; 70: 1490–1495.CrossRefGoogle ScholarPubMed
79.Nie, H, Xiong, L, Lao, N et al. . Hyperbaric oxygen preconditioning induces tolerance against spinal cord ischemia by upregulation of antioxidant enzymes in rabbits. J Cereb Blood Flow Metab 2006; 26: 666–674.CrossRefGoogle ScholarPubMed
80.Kakinohana, M, Harada, H, Mishima, Y, Kano, T, Sugahara, K. Neuroprotective effect of epidural electrical stimulation against ischemic spinal cord injury in rats: electrical preconditioning. Anesthesiology 2005; 103: 84–92.CrossRefGoogle ScholarPubMed
81.Hu, G, Salem, MR, Crystal, GJ. Role of adenosine receptors in volatile anesthetic preconditioning against neutrophil-induced contractile dysfunction in isolated rat hearts. Anesthesiology 2005; 103: 287–295.CrossRefGoogle ScholarPubMed
82.Hu, G, Vasiliauskas, T, Salem, MR, Rhone, DP, Crystal, GJ. Neutrophils pretreated with volatile anesthetics lose ability to cause cardiac dysfunction. Anesthesiology 2003; 98: 712–718.CrossRefGoogle ScholarPubMed
83.Mobert, J, Zahler, S, Becker, BF, Conzen, PF. Inhibition of neutrophil activation by volatile anesthetics decreases adhesion to cultured human endothelial cells. Anesthesiology 1999; 90: 1372–1381.CrossRefGoogle ScholarPubMed
84.Novalija, E, Fujita, S, Kampine, JP, Stowe, DF. Sevoflurane mimics ischemic preconditioning effects on coronary flow and nitric oxide release in isolated hearts. Anesthesiology 1999; 91: 701–712.CrossRefGoogle ScholarPubMed
85.de Klaver, MJ, Buckingham, MG, Rich, GF. Isoflurane pretreatment has immediate and delayed protective effects against cytokine-induced injury in endothelial and vascular smooth muscle cells. Anesthesiology 2003; 99: 896–903.CrossRefGoogle ScholarPubMed
86.Heindl, B, Becker, BF, Zahler, S, Conzen, PF. Volatile anaesthetics reduce adhesion of blood platelets under low-flow conditions in the coronary system of isolated guinea pig hearts. Acta Anaesthesiol Scand 1998; 42: 995–1003.CrossRefGoogle ScholarPubMed
87.Heindl, B, Conzen, PF, Becker, BF. The volatile anesthetic sevoflurane mitigates cardiodepressive effects of platelets in reperfused hearts. Basic Res Cardiol 1999; 94: 102–111.CrossRefGoogle ScholarPubMed
88.Hu, G, Salem, MR, Crystal, GJ. Isoflurane prevents platelets from enhancing neutrophil-induced coronary endothelial dysfunction. Anesth Analg 2005; 101: 1261–1268.CrossRefGoogle ScholarPubMed
89.Garcia, C, Julier, K, Bestmann, L et al. . Preconditioning with sevoflurane decreases PECAM-1 expression and improves one-year cardiovascular outcome in coronary artery bypass graft surgery. Br J Anaesth 2005; 94: 159–165.CrossRefGoogle ScholarPubMed
90.Zaugg, M, Lucchinetti, E, Garcia, C et al. . Anaesthetics and cardiac preconditioning. Part II. Clinical implications. Br J Anaesth 2003; 91: 566–576.CrossRefGoogle ScholarPubMed
91.Shayevitz, JR, Rodriguez, JL, Gilligan, L, Johnson, KJ, Tait, AR. Volatile anesthetic modulation of lung injury and outcome in a murine model of multiple organ dysfunction syndrome. Shock 1995; 4: 61–67.CrossRefGoogle Scholar
92.Reutershan, J, Chang, D, Hayes, JK, Ley, K. Protective effects of isoflurane pretreatment in endotoxin-induced lung injury. Anesthesiology 2006; 104: 511–517.CrossRefGoogle ScholarPubMed
93.Giraud, O, Seince, PF, Rolland, C et al. . Halothane reduces the early lipopolysaccharide-induced lung inflammation in mechanically ventilated rats. Am J Respir Crit Care Med 2000; 162: 2278–2286.CrossRefGoogle ScholarPubMed
94.Shayevitz, JR, Varani, J, Ward, PA, Knight, PR. Halothane and isoflurane increase pulmonary artery endothelial cell sensitivity to oxidant-mediated injury. Anesthesiology 1991; 74: 1067–1077.CrossRefGoogle ScholarPubMed
95.Liu, R, Ishibe, Y, Ueda, M. Isoflurane-sevoflurane administration before ischemia attenuates ischemia–reperfusion-induced injury in isolated rat lungs. Anesthesiology 2000; 92: 833–840.CrossRefGoogle ScholarPubMed
96.Julier, K, da Silva, R, Garcia, C et al. . Preconditioning by sevoflurane decreases biochemical markers for myocardial and renal dysfunction in coronary artery bypass graft surgery: a double-blinded, placebo-controlled, multicenter study. Anesthesiology 2003; 98: 1315–1327.CrossRefGoogle ScholarPubMed
97.Pathak, BL, Becker, GL, Reilly, PJ, Hanson, KA, Landers, DF. Isoflurane partially preserves energy balance in isolated hepatocytes during in vitro anoxia. Anesth Analg 1991; 72: 571–577.CrossRefGoogle ScholarPubMed
98.Li, Q, Yu, WF, Zhou, MT et al. . Isoflurane preserves energy balance in isolated hepatocytes during in vitro anoxia/reoxygenation. World J Gastroenterol 2005; 11: 3920–3924.CrossRefGoogle ScholarPubMed
99.Kon, S, Imai, M, Inaba, H. Isoflurane attenuates early neutrophil-independent hypoxia-reoxygenation injuries in the reperfused liver in fasted rats. Anesthesiology 1997; 86: 128–136.CrossRefGoogle ScholarPubMed
100.Hoetzel, A, Geiger, S, Loop, T et al. . Differential effects of volatile anesthetics on hepatic heme oxygenase-1 expression in the rat. Anesthesiology 2002; 97: 1318–1321.CrossRefGoogle ScholarPubMed
101.Hoetzel, A, Leitz, D, Schmidt, R et al. . Mechanism of hepatic heme oxygenase-1 induction by isoflurane. Anesthesiology 2006; 104: 101–109.CrossRefGoogle ScholarPubMed
102.Pannen, BH, Kohler, N, Hole, B et al. . Protective role of endogenous carbon monoxide in hepatic microcirculatory dysfunction after hemorrhagic shock in rats. J Clin Invest 1998; 102: 1220–1228.CrossRefGoogle ScholarPubMed
103.Kato, H, Amersi, F, Buelow, R et al. . Heme oxygenase-1 overexpression protects rat livers from ischemia/reperfusion injury with extended cold preservation. Am J Transplant 2001; 1: 121–128.CrossRefGoogle ScholarPubMed
104.Patel, A, van de Poll, MC, Greve, JW et al. . Early stress protein gene expression in a human model of ischemic preconditioning. Transplantation 2004; 78: 1479–1487.CrossRefGoogle Scholar
105.Lai, IR, Ma, MC, Chen, CF, Chang, KJ. The protective role of heme oxygenase-1 on the liver after hypoxic preconditioning in rats. Transplantation 2004; 77: 1004–1008.CrossRefGoogle ScholarPubMed
106.Terajima, H, Enders, G, Thiaener, A et al. . Impact of hyperthermic preconditioning on postischemic hepatic microcirculatory disturbances in an isolated perfusion model of the rat liver. Hepatology 2000; 31: 407–415.CrossRefGoogle Scholar
107.Lu, R, Peng, J, Xiao, L, Deng, HW, Li, YJ. Heme oxygenase-1 pathway is involved in delayed protection induced by heat stress against cardiac ischemia–reperfusion injury. Int J Cardiol 2002; 82: 133–140.CrossRefGoogle ScholarPubMed
108.McNally, SJ, Harrison, EM, Ross, JA, Garden, OJ, Wigmore, SJ. Curcumin induces heme oxygenase-1 in hepatocytes and is protective in simulated cold preservation and warm reperfusion injury. Transplantation 2006; 81: 623–626.CrossRefGoogle ScholarPubMed
109.Li, QF, Wang, XR, Yang, YW, Su, DS. Up-regulation of hypoxia inducible factor 1alpha by isoflurane in Hep3B cells. Anesthesiology 2006; 105: 1211–1219.CrossRefGoogle ScholarPubMed
110.Wang, C, Weihrauch, D, Schwabe, DA et al. . Extracellular signal-regulated kinases trigger isoflurane preconditioning concomitant with upregulation of hypoxia-inducible factor-1alpha and vascular endothelial growth factor expression in rats. Anesth Analg 2006; 103: 281–288.CrossRefGoogle ScholarPubMed
111.Hartman, JC, Pagel, PS, Proctor, LT et al. . Influence of desflurane, isoflurane and halothane on regional tissue perfusion in dogs. Can J Anaesth 1992; 39: 877–887.CrossRefGoogle ScholarPubMed
112.O’Riordan, J, O'Beirne, HA, Young, Y, Bellamy, MC. Effects of desflurane and isoflurane on splanchnic microcirculation during major surgery. Br J Anaesth 1997; 78: 95–96.CrossRefGoogle ScholarPubMed
113.Hayes, JK, Havaleshko, DM, Plachinta, RV, Rich, GF. Isoflurane pretreatment supports hemodynamics and leukocyte rolling velocities in rat mesentery during lipopolysaccharide-induced inflammation. Anesth Analg 2004; 98: 999–1006table of contents.CrossRefGoogle ScholarPubMed
114.Miller, LS, Morita, Y, Rangan, U et al. . Suppression of cytokine-induced neutrophil accumulation in rat mesenteric venules in vivo by general anesthesia. Int J Microcirc Clin Exp 1996; 16: 147–154.CrossRefGoogle ScholarPubMed
115.Miura, Y, Grocott, HP, Bart, RD et al. . Differential effects of anesthetic agents on outcome from near-complete but not incomplete global ischemia in the rat. Anesthesiology 1998; 89: 391–400.CrossRefGoogle Scholar
116.Warner, DS, McFarlane, C, Todd, MM, Ludwig, P, McAllister, AM. Sevoflurane and halothane reduce focal ischemic brain damage in the rat. Possible influence on thermoregulation. Anesthesiology 1993; 79: 985–992.CrossRefGoogle ScholarPubMed
117.Baughman, VL, Hoffman, WE, Miletich, DJ, Albrecht, RF, Thomas, C. Neurologic outcome in rats following incomplete cerebral ischemia during halothane, isoflurane, or N2O. Anesthesiology 1988; 69: 192–198.CrossRefGoogle ScholarPubMed
118.Newberg, LA, Milde, JH, Michenfelder, JD. The cerebral metabolic effects of isoflurane at and above concentrations that suppress cortical electrical activity. Anesthesiology 1983; 59: 23–28.CrossRefGoogle ScholarPubMed
119.Yang, J, Zorumski, CF. Effects of isoflurane on N-methyl-d-aspartate gated ion channels in cultured rat hippocampal neurons. Ann NY Acad Sci 1991; 625: 287–289.CrossRefGoogle ScholarPubMed
120.Miao, N, Frazer, MJ, Lynch, C. Volatile anesthetics depress Ca2+ transients and glutamate release in isolated cerebral synaptosomes. Anesthesiology 1995; 83: 593–603.CrossRefGoogle ScholarPubMed
121.Quinlan, JJ, Firestone, S, Firestone, LL. Isoflurane's enhancement of chloride flux through rat brain gamma-aminobutyric acid type a receptors is stereoselective. Anesthesiology 1995; 83: 611–615.CrossRefGoogle ScholarPubMed
122.Patel, PM, Drummond, JC, Cole, DJ, Goskowicz, RL. Isoflurane reduces ischemia-induced glutamate release in rats subjected to forebrain ischemia. Anesthesiology 1995; 82: 996–1003.CrossRefGoogle ScholarPubMed
123.Warner, DS. Isoflurane neuroprotection: a passing fantasy, again? Anesthesiology 2000; 92: 1226–1228.CrossRefGoogle Scholar
124.Li, Y, Chopp, M, Jiang, N, Yao, F, Zaloga, C. Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 1995; 15: 389–397.CrossRefGoogle ScholarPubMed
125.Du, C, Hu, R, Csernansky, CA, Hsu, CY, Choi, DW. Very delayed infarction after mild focal cerebral ischemia: a role for apoptosis? J Cereb Blood Flow Metab 1996; 16: 195–201.CrossRefGoogle ScholarPubMed
126.Patel, P. No magic bullets: the ephemeral nature of anesthetic-mediated neuroprotection. Anesthesiology 2004; 100: 1049–1051.CrossRefGoogle ScholarPubMed
127.Elsersy, H, Sheng, H, Lynch, JR et al. . Effects of isoflurane versus fentanyl-nitrous oxide anesthesia on long-term outcome from severe forebrain ischemia in the rat. Anesthesiology 2004; 100: 1160–1166.CrossRefGoogle ScholarPubMed
128.Kawaguchi, M, Kimbro, JR, Drummond, JC et al. . Isoflurane delays but does not prevent cerebral infarction in rats subjected to focal ischemia. Anesthesiology 2000; 92: 1335–1342.CrossRefGoogle Scholar
129.Zheng, S, Zuo, Z. Isoflurane preconditioning reduces purkinje cell death in an in vitro model of rat cerebellar ischemia. Neuroscience 2003; 118: 99–106.CrossRefGoogle Scholar
130.Blanck, TJ, Haile, M, Xu, F et al. . Isoflurane pretreatment ameliorates postischemic neurologic dysfunction and preserves hippocampal Ca2+/calmodulin-dependent protein kinase in a canine cardiac arrest model. Anesthesiology 2000; 93: 1285–1293.CrossRefGoogle Scholar
131.Kehl, F, Payne, RS, Roewer, N, Schurr, A. Sevoflurane-induced preconditioning of rat brain in vitro and the role of katp channels. Brain Res 2004; 1021: 76–81.CrossRefGoogle ScholarPubMed
132.Kapinya, KJ, Lowl, D, Futterer, C et al. . Tolerance against ischemic neuronal injury can be induced by volatile anesthetics and is inducible NO synthase dependent. Stroke 2002; 33: 1889–1898.CrossRefGoogle ScholarPubMed
133.Park, HP, Jeon, YT, Hwang, JW et al. . Isoflurane preconditioning protects motor neurons from spinal cord ischemia: Its dose–response effects and activation of mitochondrial adenosine triphosphate-dependent potassium channel. Neurosci Lett 2005; 387: 90–94.CrossRefGoogle ScholarPubMed
134.Sang, H, Cao, L, Qiu, P et al. . Isoflurane produces delayed preconditioning against spinal cord ischemic injury via release of free radicals in rabbits. Anesthesiology 2006; 105: 953–960.CrossRefGoogle ScholarPubMed
135.Zvara, DA, Bryant, AJ, Deal, DD et al. . Anesthetic preconditioning with sevoflurane does not protect the spinal cord after an ischemic–reperfusion injury in the rat. Anesth Analg 2006; 102: 1341–1347.CrossRefGoogle Scholar