Skip to main content
Top
Published in: BMC Anesthesiology 1/2017

Open Access 01-12-2017 | Research article

Repeated remote ischemic preconditioning and isoflurane anesthesia in an experimental model of renal ischemia-reperfusion injury

Authors: Theo P. Menting, Mehmet Ergun, Moira H. D. Bruintjes, Kimberley E. Wever, Roger M. L. M. Lomme, Harry van Goor, Michiel C. Warlé

Published in: BMC Anesthesiology | Issue 1/2017

Login to get access

Abstract

Background

In animal studies, remote ischemic preconditioning (RIPC) and anesthetic preconditioning are successful in reducing renal ischemia reperfusion injury (IRI), however the protective effect of RIPC may be improved by repeating the RIPC stimulus.

Methods

Sprague-Dawley rats underwent unilateral nephrectomy followed by 30 min of renal pedicle clamping. Animals were allocated into six groups: sham, control (IRI), RepISO (daily isoflurane anesthesia), RIPC (single dose isoflurane anesthesia and single dose RIPC), RepISO + RIPC (7-day isoflurane anesthesia and single dose RIPC) and RepISO + RepRIPC (7-day isoflurane anesthesia with 7-day RIPC). RIPC was applied by 3×5 min of cuff inflation on both thighs. Serum creatinine and urea levels were measured and histology was obtained at day two.

Results

RepISO diminished renal IRI, as reflected by a significant reduction in serum creatinine levels as compared to the control group, 170 ± 74 resp. 107 ± 29 μmol/L. The other preconditioning protocols showed similar reduction in serum creatinine levels as compared to the control group. No significant differences were observed between the different preconditioning protocols. For urea levels, only RepISO + RIPC resulted in significantly lower levels as compared to the control group, 14 ± 4 resp. 22 ± 7 mmol/L (p = 0.010). In the preconditioning groups only RepISO showed less histological damage as compared to controls 1.73 ± 1.19 resp. 2.91 ± 1.22 (p = 0.032).

Conclusions

In this study no additional protective effect of repeated ischemic preconditioning was observed as compared to single dose RIPC. Repeated administration of isoflurane provided stronger protection against renal IRI as compared to single dose isoflurane.
Literature
2.
go back to reference Piper HM, Garcia-Dorado D, Ovize M. A fresh look at reperfusion injury. Cardiovasc Res. 1998;38(2):291–300.CrossRefPubMed Piper HM, Garcia-Dorado D, Ovize M. A fresh look at reperfusion injury. Cardiovasc Res. 1998;38(2):291–300.CrossRefPubMed
3.
go back to reference Ong SB, et al. The mitochondrial permeability transition pore and its role in myocardial ischemia reperfusion injury. J Mol Cell Cardiol. 2015;78:23–34.CrossRefPubMed Ong SB, et al. The mitochondrial permeability transition pore and its role in myocardial ischemia reperfusion injury. J Mol Cell Cardiol. 2015;78:23–34.CrossRefPubMed
5.
go back to reference Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74(5):1124–36.CrossRefPubMed Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74(5):1124–36.CrossRefPubMed
6.
go back to reference Przyklenk K, et al. Regional ischemic ‘preconditioning’ protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation. 1993;87(3):893–9.CrossRefPubMed Przyklenk K, et al. Regional ischemic ‘preconditioning’ protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation. 1993;87(3):893–9.CrossRefPubMed
7.
go back to reference Cochrane J, et al. Ischemic preconditioning attenuates functional, metabolic, and morphologic injury from ischemic acute renal failure in the rat. Ren Fail. 1999;21(2):135–45.CrossRefPubMed Cochrane J, et al. Ischemic preconditioning attenuates functional, metabolic, and morphologic injury from ischemic acute renal failure in the rat. Ren Fail. 1999;21(2):135–45.CrossRefPubMed
8.
go back to reference Liang Y, et al. Isoflurane preconditioning ameliorates renal ischemia-reperfusion injury through antiinflammatory and antiapoptotic actions in rats. Biol Pharm Bull. 2014;37(10):1599–605.CrossRefPubMed Liang Y, et al. Isoflurane preconditioning ameliorates renal ischemia-reperfusion injury through antiinflammatory and antiapoptotic actions in rats. Biol Pharm Bull. 2014;37(10):1599–605.CrossRefPubMed
9.
go back to reference Muntean DM, et al. Volatile anaesthetics and cardioprotection: lessons from animal studies. Fundam Clin Pharmacol. 2013;27(1):21–34.CrossRefPubMed Muntean DM, et al. Volatile anaesthetics and cardioprotection: lessons from animal studies. Fundam Clin Pharmacol. 2013;27(1):21–34.CrossRefPubMed
10.
go back to reference Redel A, et al. Comparison of isoflurane-, sevoflurane-, and desflurane-induced pre- and postconditioning against myocardial infarction in mice in vivo. Exp Biol Med (Maywood). 2009;234(10):1186–91.CrossRef Redel A, et al. Comparison of isoflurane-, sevoflurane-, and desflurane-induced pre- and postconditioning against myocardial infarction in mice in vivo. Exp Biol Med (Maywood). 2009;234(10):1186–91.CrossRef
11.
go back to reference Davis RF, et al. The effect of halothane anesthesia on myocardial necrosis, hemodynamic performance, and regional myocardial blood flow in dogs following coronary artery occlusion. Anesthesiology. 1983;59(5):402–11.CrossRefPubMed Davis RF, et al. The effect of halothane anesthesia on myocardial necrosis, hemodynamic performance, and regional myocardial blood flow in dogs following coronary artery occlusion. Anesthesiology. 1983;59(5):402–11.CrossRefPubMed
12.
go back to reference Zaugg M, et al. Anesthetic cardioprotection in clinical practice from proof-of-concept to clinical applications. Curr Pharm Des. 2014;20(36):5706–26.CrossRefPubMed Zaugg M, et al. Anesthetic cardioprotection in clinical practice from proof-of-concept to clinical applications. Curr Pharm Des. 2014;20(36):5706–26.CrossRefPubMed
13.
go back to reference Zaugg M, et al. Differential effects of anesthetics on mitochondrial K(ATP) channel activity and cardiomyocyte protection. Anesthesiology. 2002;97(1):15–23.CrossRefPubMed Zaugg M, et al. Differential effects of anesthetics on mitochondrial K(ATP) channel activity and cardiomyocyte protection. Anesthesiology. 2002;97(1):15–23.CrossRefPubMed
14.
go back to reference Mullenheim J, et al. Ketamine, but not S(+)-ketamine, blocks ischemic preconditioning in rabbit hearts in vivo. Anesthesiology. 2001;94(4):630–6.CrossRefPubMed Mullenheim J, et al. Ketamine, but not S(+)-ketamine, blocks ischemic preconditioning in rabbit hearts in vivo. Anesthesiology. 2001;94(4):630–6.CrossRefPubMed
15.
go back to reference Cope DK, et al. Volatile anesthetics protect the ischemic rabbit myocardium from infarction. Anesthesiology. 1997;86(3):699–709.CrossRefPubMed Cope DK, et al. Volatile anesthetics protect the ischemic rabbit myocardium from infarction. Anesthesiology. 1997;86(3):699–709.CrossRefPubMed
16.
go back to reference Kohro S, et al. Anesthetic effects on mitochondrial ATP-sensitive K channel. Anesthesiology. 2001;95(6):1435–340.CrossRefPubMed Kohro S, et al. Anesthetic effects on mitochondrial ATP-sensitive K channel. Anesthesiology. 2001;95(6):1435–340.CrossRefPubMed
18.
go back to reference Hausenloy DJ, et al. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet. 2007;370(9587):575–9.CrossRefPubMed Hausenloy DJ, et al. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet. 2007;370(9587):575–9.CrossRefPubMed
19.
go back to reference Walsh SR, et al. Ischaemic preconditioning during cardiac surgery: systematic review and meta-analysis of perioperative outcomes in randomised clinical trials. Eur J Cardiothorac Surg. 2008;34(5):985–94.CrossRefPubMed Walsh SR, et al. Ischaemic preconditioning during cardiac surgery: systematic review and meta-analysis of perioperative outcomes in randomised clinical trials. Eur J Cardiothorac Surg. 2008;34(5):985–94.CrossRefPubMed
20.
go back to reference Meng R, et al. Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology. 2012;79(18):1853–61.CrossRefPubMed Meng R, et al. Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology. 2012;79(18):1853–61.CrossRefPubMed
21.
go back to reference Jones H, et al. Seven-day remote ischemic preconditioning improves local and systemic endothelial function and microcirculation in healthy humans. Am J Hypertens. 2014;27(7):918–25.CrossRefPubMed Jones H, et al. Seven-day remote ischemic preconditioning improves local and systemic endothelial function and microcirculation in healthy humans. Am J Hypertens. 2014;27(7):918–25.CrossRefPubMed
22.
go back to reference Jablonski P, et al. An experimental model for assessment of renal recovery from warm ischemia. Transplantation. 1983;35(3):198–204.CrossRefPubMed Jablonski P, et al. An experimental model for assessment of renal recovery from warm ischemia. Transplantation. 1983;35(3):198–204.CrossRefPubMed
23.
go back to reference Wever KE, et al. Local and remote ischemic postconditionings have synergistic protective effects on renal ischemia-reperfusion injury. Transplantation. 2012;94(1):e1–2.CrossRefPubMed Wever KE, et al. Local and remote ischemic postconditionings have synergistic protective effects on renal ischemia-reperfusion injury. Transplantation. 2012;94(1):e1–2.CrossRefPubMed
24.
go back to reference Wever KE, et al. Remote ischaemic preconditioning by brief hind limb ischaemia protects against renal ischaemia-reperfusion injury: the role of adenosine. Nephrol Dial Transplant. 2011;26(10):3108–17.CrossRefPubMed Wever KE, et al. Remote ischaemic preconditioning by brief hind limb ischaemia protects against renal ischaemia-reperfusion injury: the role of adenosine. Nephrol Dial Transplant. 2011;26(10):3108–17.CrossRefPubMed
25.
go back to reference Burne MJ, et al. Genetic susceptibility to renal ischemia reperfusion injury revealed in a murine model. Transplantation. 2000;69(5):1023–5.CrossRefPubMed Burne MJ, et al. Genetic susceptibility to renal ischemia reperfusion injury revealed in a murine model. Transplantation. 2000;69(5):1023–5.CrossRefPubMed
26.
go back to reference Guo Y, et al. Genetic background, gender, age, body temperature, and arterial blood pH have a major impact on myocardial infarct size in the mouse and need to be carefully measured and/or taken into account: results of a comprehensive analysis of determinants of infarct size in 1,074 mice. Basic Res Cardiol. 2012;107(5):288.CrossRefPubMedPubMedCentral Guo Y, et al. Genetic background, gender, age, body temperature, and arterial blood pH have a major impact on myocardial infarct size in the mouse and need to be carefully measured and/or taken into account: results of a comprehensive analysis of determinants of infarct size in 1,074 mice. Basic Res Cardiol. 2012;107(5):288.CrossRefPubMedPubMedCentral
27.
go back to reference Ali ZA, et al. Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial. Circulation. 2007;116(11 Suppl):I98–105.PubMed Ali ZA, et al. Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial. Circulation. 2007;116(11 Suppl):I98–105.PubMed
28.
go back to reference Wei M, et al. Repeated remote ischemic postconditioning protects against adverse left ventricular remodeling and improves survival in a rat model of myocardial infarction. Circ Res. 2011;108(10):1220–5.CrossRefPubMed Wei M, et al. Repeated remote ischemic postconditioning protects against adverse left ventricular remodeling and improves survival in a rat model of myocardial infarction. Circ Res. 2011;108(10):1220–5.CrossRefPubMed
29.
go back to reference Rohailla S, et al. Acute, delayed and chronic remote ischemic conditioning is associated with downregulation of mTOR and enhanced autophagy signaling. PLoS One. 2014;9(10):e111291.CrossRefPubMedPubMedCentral Rohailla S, et al. Acute, delayed and chronic remote ischemic conditioning is associated with downregulation of mTOR and enhanced autophagy signaling. PLoS One. 2014;9(10):e111291.CrossRefPubMedPubMedCentral
30.
go back to reference Liang Y, et al. Long-term, regular remote ischemic preconditioning improves endothelial function in patients with coronary heart disease. Braz J Med Biol Res. 2015;48(6):568–76.CrossRefPubMedPubMedCentral Liang Y, et al. Long-term, regular remote ischemic preconditioning improves endothelial function in patients with coronary heart disease. Braz J Med Biol Res. 2015;48(6):568–76.CrossRefPubMedPubMedCentral
Metadata
Title
Repeated remote ischemic preconditioning and isoflurane anesthesia in an experimental model of renal ischemia-reperfusion injury
Authors
Theo P. Menting
Mehmet Ergun
Moira H. D. Bruintjes
Kimberley E. Wever
Roger M. L. M. Lomme
Harry van Goor
Michiel C. Warlé
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Anesthesiology / Issue 1/2017
Electronic ISSN: 1471-2253
DOI
https://doi.org/10.1186/s12871-017-0310-x

Other articles of this Issue 1/2017

BMC Anesthesiology 1/2017 Go to the issue