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Published in: Basic Research in Cardiology 1/2015

Open Access 01-01-2015 | Review

Remote ischemic conditioning: from experimental observation to clinical application: report from the 8th Biennial Hatter Cardiovascular Institute Workshop

Authors: Jack M. J. Pickard, Hans Erik Bøtker, Gabriele Crimi, Brian Davidson, Sean M. Davidson, David Dutka, Peter Ferdinandy, Rocky Ganske, David Garcia-Dorado, Zoltan Giricz, Alexander V. Gourine, Gerd Heusch, Rajesh Kharbanda, Petra Kleinbongard, Raymond MacAllister, Christopher McIntyre, Patrick Meybohm, Fabrice Prunier, Andrew Redington, Nicola J. Robertson, M. Saadeh Suleiman, Andrew Vanezis, Stewart Walsh, Derek M. Yellon, Derek J. Hausenloy

Published in: Basic Research in Cardiology | Issue 1/2015

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Abstract

In 1993, Przyklenk and colleagues made the intriguing experimental observation that ‘brief ischemia in one vascular bed also protects remote, virgin myocardium from subsequent sustained coronary artery occlusion’ and that this effect ‘…. may be mediated by factor(s) activated, produced, or transported throughout the heart during brief ischemia/reperfusion’. This seminal study laid the foundation for the discovery of ‘remote ischemic conditioning’ (RIC), a phenomenon in which the heart is protected from the detrimental effects of acute ischemia/reperfusion injury (IRI), by applying cycles of brief ischemia and reperfusion to an organ or tissue remote from the heart. The concept of RIC quickly evolved to extend beyond the heart, encompassing inter-organ protection against acute IRI. The crucial discovery that the protective RIC stimulus could be applied non-invasively, by simply inflating and deflating a blood pressure cuff placed on the upper arm to induce cycles of brief ischemia and reperfusion, has facilitated the translation of RIC into the clinical setting. Despite intensive investigation over the last 20 years, the underlying mechanisms continue to elude researchers. In the 8th Biennial Hatter Cardiovascular Institute Workshop, recent developments in the field of RIC were discussed with a focus on new insights into the underlying mechanisms, the diversity of non-cardiac protection, new clinical applications, and large outcome studies. The scientific advances made in this field of research highlight the journey that RIC has made from being an intriguing experimental observation to a clinical application with patient benefit.
Literature
2.
go back to reference Abu-Amara M, Yang SY, Quaglia A, Rowley P, Fuller B, Seifalian A, Davidson B (2011) Role of endothelial nitric oxide synthase in remote ischemic preconditioning of the mouse liver. Liver Transpl 17:610–619. doi:10.1002/lt.22272 PubMedCrossRef Abu-Amara M, Yang SY, Quaglia A, Rowley P, Fuller B, Seifalian A, Davidson B (2011) Role of endothelial nitric oxide synthase in remote ischemic preconditioning of the mouse liver. Liver Transpl 17:610–619. doi:10.​1002/​lt.​22272 PubMedCrossRef
3.
go back to reference Abu-Amara M, Yang SY, Quaglia A, Rowley P, Tapuria N, Fuller B, Davidson B, Seifalian A (2012) The hepatic soluble guanylyl cyclase-cyclic guanosine monophosphate pathway mediates the protection of remote ischemic preconditioning on the microcirculation in liver ischemia-reperfusion injury. Transplantation 93:880–886. doi:10.1097/TP.0b013e31824cd59d PubMedCrossRef Abu-Amara M, Yang SY, Quaglia A, Rowley P, Tapuria N, Fuller B, Davidson B, Seifalian A (2012) The hepatic soluble guanylyl cyclase-cyclic guanosine monophosphate pathway mediates the protection of remote ischemic preconditioning on the microcirculation in liver ischemia-reperfusion injury. Transplantation 93:880–886. doi:10.​1097/​TP.​0b013e31824cd59d​ PubMedCrossRef
4.
go back to reference Ali ZA, Callaghan CJ, Lim E, Ali AA, Nouraei SA, Akthar AM, Boyle JR, Varty K, Kharbanda RK, Dutka DP, Gaunt ME (2007) Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial. Circulation 116:I98–I105. doi:10.1161/circulationaha.106.679167 PubMedCrossRef Ali ZA, Callaghan CJ, Lim E, Ali AA, Nouraei SA, Akthar AM, Boyle JR, Varty K, Kharbanda RK, Dutka DP, Gaunt ME (2007) Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial. Circulation 116:I98–I105. doi:10.​1161/​circulationaha.​106.​679167 PubMedCrossRef
5.
go back to reference Azzopardi DV, Strohm B, Edwards AD, Dyet L, Halliday HL, Juszczak E, Kapellou O, Levene M, Marlow N, Porter E, Thoresen M, Whitelaw A, Brocklehurst P (2009) Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med 361:1349–1358. doi:10.1056/NEJMoa0900854 PubMedCrossRef Azzopardi DV, Strohm B, Edwards AD, Dyet L, Halliday HL, Juszczak E, Kapellou O, Levene M, Marlow N, Porter E, Thoresen M, Whitelaw A, Brocklehurst P (2009) Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med 361:1349–1358. doi:10.​1056/​NEJMoa0900854 PubMedCrossRef
7.
go back to reference Bell RM, Rear R, Cunningham J, Dawnay A, Yellon DM (2014) Effect of remote ischaemic conditioning on contrast-induced nephropathy in patients undergoing elective coronary angiography (ERICCIN): rationale and study design of a randomised single-centre, double-blind placebo-controlled trial. Clin Res Cardiol 103:203–209. doi:10.1007/s00392-013-0637-3 PubMedCentralPubMedCrossRef Bell RM, Rear R, Cunningham J, Dawnay A, Yellon DM (2014) Effect of remote ischaemic conditioning on contrast-induced nephropathy in patients undergoing elective coronary angiography (ERICCIN): rationale and study design of a randomised single-centre, double-blind placebo-controlled trial. Clin Res Cardiol 103:203–209. doi:10.​1007/​s00392-013-0637-3 PubMedCentralPubMedCrossRef
8.
go back to reference Botker HE, Kharbanda R, Schmidt MR, Bottcher M, Kaltoft AK, Terkelsen CJ, Munk K, Andersen NH, Hansen TM, Trautner S, Lassen JF, Christiansen EH, Krusell LR, Kristensen SD, Thuesen L, Nielsen SS, Rehling M, Sorensen HT, Redington AN, Nielsen TT (2010) Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. Lancet 375:727–734. doi:10.1016/S0140-6736(09)62001-8 PubMedCrossRef Botker HE, Kharbanda R, Schmidt MR, Bottcher M, Kaltoft AK, Terkelsen CJ, Munk K, Andersen NH, Hansen TM, Trautner S, Lassen JF, Christiansen EH, Krusell LR, Kristensen SD, Thuesen L, Nielsen SS, Rehling M, Sorensen HT, Redington AN, Nielsen TT (2010) Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. Lancet 375:727–734. doi:10.​1016/​S0140-6736(09)62001-8 PubMedCrossRef
11.
go back to reference Candilio L, Malik A, Ariti C, Barnard M, Di SC, Lawrence D, Hayward M, Yap J, Roberts N, Sheikh A, Kolvekar S, Hausenloy DJ, Yellon DM (2014) Effect of remote ischaemic preconditioning on clinical outcomes in patients undergoing cardiac bypass surgery: a randomised controlled clinical trial. Heart. doi:10.1136/heartjnl-2014-306178 PubMed Candilio L, Malik A, Ariti C, Barnard M, Di SC, Lawrence D, Hayward M, Yap J, Roberts N, Sheikh A, Kolvekar S, Hausenloy DJ, Yellon DM (2014) Effect of remote ischaemic preconditioning on clinical outcomes in patients undergoing cardiac bypass surgery: a randomised controlled clinical trial. Heart. doi:10.​1136/​heartjnl-2014-306178 PubMed
12.
go back to reference Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, Van Arsdell GS, Redington AN (2006) Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol 47:2277–2282. doi:10.1016/j.jacc.2006.01.066 PubMedCrossRef Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, Van Arsdell GS, Redington AN (2006) Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol 47:2277–2282. doi:10.​1016/​j.​jacc.​2006.​01.​066 PubMedCrossRef
13.
go back to reference Contractor H, Stottrup NB, Cunnington C, Manlhiot C, Diesch J, Ormerod JO, Jensen R, Botker HE, Redington A, Schmidt MR, Ashrafian H, Kharbanda RK (2013) Aldehyde dehydrogenase-2 inhibition blocks remote preconditioning in experimental and human models. Basic Res Cardiol 108:343. doi:10.1007/s00395-013-0343-3 PubMedCrossRef Contractor H, Stottrup NB, Cunnington C, Manlhiot C, Diesch J, Ormerod JO, Jensen R, Botker HE, Redington A, Schmidt MR, Ashrafian H, Kharbanda RK (2013) Aldehyde dehydrogenase-2 inhibition blocks remote preconditioning in experimental and human models. Basic Res Cardiol 108:343. doi:10.​1007/​s00395-013-0343-3 PubMedCrossRef
14.
go back to reference Crimi G, Ferlini M, Gallo F, Sormani MP, Raineri C, Bramucci E, De Ferrari GM, Pica S, Marinoni B, Repetto A, Raisaro A, Leonardi S, Rubartelli P, Visconti LO, Ferrario M (2014) Remote ischemic postconditioning as a strategy to reduce acute kidney injury during primary PCI: a post hoc analysis of a randomized trial. Int J Cardiol. doi:10.1016/j.ijcard.2014.08.080 PubMed Crimi G, Ferlini M, Gallo F, Sormani MP, Raineri C, Bramucci E, De Ferrari GM, Pica S, Marinoni B, Repetto A, Raisaro A, Leonardi S, Rubartelli P, Visconti LO, Ferrario M (2014) Remote ischemic postconditioning as a strategy to reduce acute kidney injury during primary PCI: a post hoc analysis of a randomized trial. Int J Cardiol. doi:10.​1016/​j.​ijcard.​2014.​08.​080 PubMed
15.
go back to reference Crimi G, Pica S, Raineri C, Bramucci E, De Ferrari GM, Klersy C, Ferlini M, Marinoni B, Repetto A, Romeo M, Rosti V, Massa M, Raisaro A, Leonardi S, Rubartelli P, Oltrona VL, Ferrario M (2013) Remote ischemic post-conditioning of the lower limb during primary percutaneous coronary intervention safely reduces enzymatic infarct size in anterior myocardial infarction: a randomized controlled trial. JACC Cardiovasc Interv 6:1055–1063. doi:10.1016/j.jcin.2013.05.011 PubMedCrossRef Crimi G, Pica S, Raineri C, Bramucci E, De Ferrari GM, Klersy C, Ferlini M, Marinoni B, Repetto A, Romeo M, Rosti V, Massa M, Raisaro A, Leonardi S, Rubartelli P, Oltrona VL, Ferrario M (2013) Remote ischemic post-conditioning of the lower limb during primary percutaneous coronary intervention safely reduces enzymatic infarct size in anterior myocardial infarction: a randomized controlled trial. JACC Cardiovasc Interv 6:1055–1063. doi:10.​1016/​j.​jcin.​2013.​05.​011 PubMedCrossRef
17.
go back to reference D’Ascenzo F, Cavallero E, Moretti C, Omede P, Sciuto F, Rahman IA, Bonser RS, Yunseok J, Wagner R, Freiberger T, Kunst G, Marber MS, Thielmann M, Ji B, Amr YM, Modena MG, Zoccai GB, Sheiban I, Gaita F (2012) Remote ischaemic preconditioning in coronary artery bypass surgery: a meta-analysis. Heart 98:1267–1271. doi:10.1136/heartjnl-2011-301551 PubMedCrossRef D’Ascenzo F, Cavallero E, Moretti C, Omede P, Sciuto F, Rahman IA, Bonser RS, Yunseok J, Wagner R, Freiberger T, Kunst G, Marber MS, Thielmann M, Ji B, Amr YM, Modena MG, Zoccai GB, Sheiban I, Gaita F (2012) Remote ischaemic preconditioning in coronary artery bypass surgery: a meta-analysis. Heart 98:1267–1271. doi:10.​1136/​heartjnl-2011-301551 PubMedCrossRef
18.
go back to reference D’Ascenzo F, Moretti C, Omede P, Cerrato E, Cavallero E, Er F, Presutti DG, Colombo F, Crimi G, Conrotto F, Dinicolantonio JJ, Chen S, Prasad A, Biondi ZG, Gaita F (2014) Cardiac remote ischaemic preconditioning reduces periprocedural myocardial infarction for patients undergoing percutaneous coronary interventions: a meta-analysis of randomised clinical trials. EuroIntervention 9:1463–1471. doi:10.4244/EIJV9I12A244 PubMedCrossRef D’Ascenzo F, Moretti C, Omede P, Cerrato E, Cavallero E, Er F, Presutti DG, Colombo F, Crimi G, Conrotto F, Dinicolantonio JJ, Chen S, Prasad A, Biondi ZG, Gaita F (2014) Cardiac remote ischaemic preconditioning reduces periprocedural myocardial infarction for patients undergoing percutaneous coronary interventions: a meta-analysis of randomised clinical trials. EuroIntervention 9:1463–1471. doi:10.​4244/​EIJV9I12A244 PubMedCrossRef
19.
go back to reference Davidson SM, Selvaraj P, He D, Boi-Doku C, Yellon RL, Vicencio JM, Yellon DM (2013) Remote ischaemic preconditioning involves signalling through the SDF-1alpha/CXCR4 signalling axis. Basic Res Cardiol 108:377. doi:10.1007/s00395-013-0377-6 PubMedCrossRef Davidson SM, Selvaraj P, He D, Boi-Doku C, Yellon RL, Vicencio JM, Yellon DM (2013) Remote ischaemic preconditioning involves signalling through the SDF-1alpha/CXCR4 signalling axis. Basic Res Cardiol 108:377. doi:10.​1007/​s00395-013-0377-6 PubMedCrossRef
20.
go back to reference Davies WR, Brown AJ, Watson W, McCormick LM, West NE, Dutka DP, hoole SP (2013) Remote ischemic preconditioning improves outcome at 6 years after elective percutaneous coronary intervention: the crisp stent trial long-term follow-up. Circ Cardiovasc Interv 6:246–251. doi:10.1161/CIRCINTERVENTIONS.112.000184 PubMedCrossRef Davies WR, Brown AJ, Watson W, McCormick LM, West NE, Dutka DP, hoole SP (2013) Remote ischemic preconditioning improves outcome at 6 years after elective percutaneous coronary intervention: the crisp stent trial long-term follow-up. Circ Cardiovasc Interv 6:246–251. doi:10.​1161/​CIRCINTERVENTION​S.​112.​000184 PubMedCrossRef
21.
go back to reference Dickson EW, Reinhardt CP, Renzi FP, Becker RC, Porcaro WA, Heard SO (1999) Ischemic preconditioning may be transferable via whole blood transfusion: preliminary evidence. J Thromb Thrombolysis 8:123–129. doi:10.1023/A:1008911101951 PubMedCrossRef Dickson EW, Reinhardt CP, Renzi FP, Becker RC, Porcaro WA, Heard SO (1999) Ischemic preconditioning may be transferable via whole blood transfusion: preliminary evidence. J Thromb Thrombolysis 8:123–129. doi:10.​1023/​A:​1008911101951 PubMedCrossRef
23.
go back to reference Dong JH, Liu YX, Ji ES, He RR (2004) Limb ischemic preconditioning reduces infarct size following myocardial ischemia-reperfusion in rats. Sheng Li Xue Bao 56:41–46PubMed Dong JH, Liu YX, Ji ES, He RR (2004) Limb ischemic preconditioning reduces infarct size following myocardial ischemia-reperfusion in rats. Sheng Li Xue Bao 56:41–46PubMed
24.
go back to reference Er F, Nia AM, Dopp H, Hellmich M, Dahlem KM, Caglayan E, Kubacki T, Benzing T, Erdmann E, Burst V, Gassanov N (2012) Ischemic preconditioning for prevention of contrast medium-induced nephropathy: randomized pilot RenPro Trial (Renal Protection Trial). Circulation 126:296–303. doi:10.1161/CIRCULATIONAHA.112.096370 PubMedCrossRef Er F, Nia AM, Dopp H, Hellmich M, Dahlem KM, Caglayan E, Kubacki T, Benzing T, Erdmann E, Burst V, Gassanov N (2012) Ischemic preconditioning for prevention of contrast medium-induced nephropathy: randomized pilot RenPro Trial (Renal Protection Trial). Circulation 126:296–303. doi:10.​1161/​CIRCULATIONAHA.​112.​096370 PubMedCrossRef
25.
go back to reference Ferdinandy P, Hausenloy DJ, Heusch G, Baxter GF, Schulz R (2014) Interaction of risk factors, comorbidities, and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning. Pharmacol Rev 66:1142–1174. doi:10.1124/pr.113.008300 PubMedCrossRef Ferdinandy P, Hausenloy DJ, Heusch G, Baxter GF, Schulz R (2014) Interaction of risk factors, comorbidities, and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning. Pharmacol Rev 66:1142–1174. doi:10.​1124/​pr.​113.​008300 PubMedCrossRef
28.
30.
go back to reference Hajrasouliha AR, Tavakoli S, Ghasemi M, Jabehdar-Maralani P, Sadeghipour H, Ebrahimi F, Dehpour AR (2008) Endogenous cannabinoids contribute to remote ischemic preconditioning via cannabinoid CB2 receptors in the rat heart. Eur J Pharmacol 579:246–252. doi:10.1016/j.ejphar.2007.09.034 PubMedCrossRef Hajrasouliha AR, Tavakoli S, Ghasemi M, Jabehdar-Maralani P, Sadeghipour H, Ebrahimi F, Dehpour AR (2008) Endogenous cannabinoids contribute to remote ischemic preconditioning via cannabinoid CB2 receptors in the rat heart. Eur J Pharmacol 579:246–252. doi:10.​1016/​j.​ejphar.​2007.​09.​034 PubMedCrossRef
32.
go back to reference Hausenloy DJ, Baxter G, Bell R, Botker HE, Davidson SM, Downey J, Heusch G, Kitakaze M, Lecour S, Mentzer R, Mocanu MM, Ovize M, Schulz R, Shannon R, Walker M, Walkinshaw G, Yellon DM (2010) Translating novel strategies for cardioprotection: the Hatter Workshop Recommendations. Basic Res Cardiol 105:677–686. doi:10.1007/s00395-010-0121-4 PubMedCentralPubMedCrossRef Hausenloy DJ, Baxter G, Bell R, Botker HE, Davidson SM, Downey J, Heusch G, Kitakaze M, Lecour S, Mentzer R, Mocanu MM, Ovize M, Schulz R, Shannon R, Walker M, Walkinshaw G, Yellon DM (2010) Translating novel strategies for cardioprotection: the Hatter Workshop Recommendations. Basic Res Cardiol 105:677–686. doi:10.​1007/​s00395-010-0121-4 PubMedCentralPubMedCrossRef
33.
go back to reference Hausenloy DJ, Candilio L, Laing C, Kunst G, Pepper J, Kolvekar S, Evans R, Robertson S, Knight R, Ariti C, Clayton T, Yellon DM (2012) Effect of remote ischemic preconditioning on clinical outcomes in patients undergoing coronary artery bypass graft surgery (ERICCA): rationale and study design of a multi-centre randomized double-blinded controlled clinical trial. Clin Res Cardiol 101:339–348. doi:10.1007/s00392-011-0397-x PubMedCrossRef Hausenloy DJ, Candilio L, Laing C, Kunst G, Pepper J, Kolvekar S, Evans R, Robertson S, Knight R, Ariti C, Clayton T, Yellon DM (2012) Effect of remote ischemic preconditioning on clinical outcomes in patients undergoing coronary artery bypass graft surgery (ERICCA): rationale and study design of a multi-centre randomized double-blinded controlled clinical trial. Clin Res Cardiol 101:339–348. doi:10.​1007/​s00392-011-0397-x PubMedCrossRef
34.
go back to reference Hausenloy DJ, Erik BH, Condorelli G, Ferdinandy P, Garcia-Dorado D, Heusch G, Lecour S, van Laake LW, Madonna R, Ruiz-Meana M, Schulz R, Sluijter JP, Yellon DM, Ovize M (2013) Translating cardioprotection for patient benefit: position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res 98:7–27. doi:10.1093/cvr/cvt004 PubMedCrossRef Hausenloy DJ, Erik BH, Condorelli G, Ferdinandy P, Garcia-Dorado D, Heusch G, Lecour S, van Laake LW, Madonna R, Ruiz-Meana M, Schulz R, Sluijter JP, Yellon DM, Ovize M (2013) Translating cardioprotection for patient benefit: position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res 98:7–27. doi:10.​1093/​cvr/​cvt004 PubMedCrossRef
35.
go back to reference Hausenloy DJ, Mwamure PK, Venugopal V, Harris J, Barnard M, Grundy E, Ashley E, Vichare S, Di Salvo C, Kolvekar S, Hayward M, Keogh B, MacAllister RJ, Yellon DM (2007) Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet 370:575–579. doi:10.1016/S0140-6736(07)61296-3 PubMedCrossRef Hausenloy DJ, Mwamure PK, Venugopal V, Harris J, Barnard M, Grundy E, Ashley E, Vichare S, Di Salvo C, Kolvekar S, Hayward M, Keogh B, MacAllister RJ, Yellon DM (2007) Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet 370:575–579. doi:10.​1016/​S0140-6736(07)61296-3 PubMedCrossRef
42.
go back to reference Hong DM, Lee EH, Kim HJ, Min JJ, Chin JH, Choi DK, Bahk JH, Sim JY, Choi IC, Jeon Y (2014) Does remote ischaemic preconditioning with postconditioning improve clinical outcomes of patients undergoing cardiac surgery? Remote ischaemic preconditioning with postconditioning outcome trial. Eur Heart J 35:176–183. doi:10.1093/eurheartj/eht346 PubMedCrossRef Hong DM, Lee EH, Kim HJ, Min JJ, Chin JH, Choi DK, Bahk JH, Sim JY, Choi IC, Jeon Y (2014) Does remote ischaemic preconditioning with postconditioning improve clinical outcomes of patients undergoing cardiac surgery? Remote ischaemic preconditioning with postconditioning outcome trial. Eur Heart J 35:176–183. doi:10.​1093/​eurheartj/​eht346 PubMedCrossRef
43.
go back to reference Hoole S, Heck PM, Sharples L, Khan SN, Duehmke R, Densem CG, Clarke SC, Shapiro LM, Schofield PM, O’Sullivan M, Dutka DP (2009) Cardiac Remote Ischemic Preconditioning in Coronary Stenting (CRISP Stent) Study: a prospective, randomized control trial. Circulation 119:820–827. doi:10.1161/CIRCULATIONAHA.108.809723 PubMedCrossRef Hoole S, Heck PM, Sharples L, Khan SN, Duehmke R, Densem CG, Clarke SC, Shapiro LM, Schofield PM, O’Sullivan M, Dutka DP (2009) Cardiac Remote Ischemic Preconditioning in Coronary Stenting (CRISP Stent) Study: a prospective, randomized control trial. Circulation 119:820–827. doi:10.​1161/​CIRCULATIONAHA.​108.​809723 PubMedCrossRef
44.
go back to reference Hougaard KD, Hjort N, Zeidler D, Sorensen L, Norgaard A, Thomsen RB, Jonsdottir K, Mouridsen K, Hansen TM, Cho TH, Nielsen TT, Botker HE, Ostergaard L, Andersen G (2013) Remote ischemic perconditioning in thrombolysed stroke patients: randomized study of activating endogenous neuroprotection-design and MRI measurements. Int J Stroke 8:141–146. doi:10.1111/j.1747-4949.2012.00786.x PubMedCrossRef Hougaard KD, Hjort N, Zeidler D, Sorensen L, Norgaard A, Thomsen RB, Jonsdottir K, Mouridsen K, Hansen TM, Cho TH, Nielsen TT, Botker HE, Ostergaard L, Andersen G (2013) Remote ischemic perconditioning in thrombolysed stroke patients: randomized study of activating endogenous neuroprotection-design and MRI measurements. Int J Stroke 8:141–146. doi:10.​1111/​j.​1747-4949.​2012.​00786.​x PubMedCrossRef
45.
go back to reference Iliodromitis EK, Kyrzopoulos S, Paraskevaidis IA, Kolocassides KG, Adamopoulos S, Karavolias G, Kremastinos DT (2006) Increased C reactive protein and cardiac enzyme levels after coronary stent implantation. Is there protection by remote ischaemic preconditioning? Heart 92:1821–1826. doi:10.1136/hrt.2006.089060 PubMedCentralPubMedCrossRef Iliodromitis EK, Kyrzopoulos S, Paraskevaidis IA, Kolocassides KG, Adamopoulos S, Karavolias G, Kremastinos DT (2006) Increased C reactive protein and cardiac enzyme levels after coronary stent implantation. Is there protection by remote ischaemic preconditioning? Heart 92:1821–1826. doi:10.​1136/​hrt.​2006.​089060 PubMedCentralPubMedCrossRef
46.
go back to reference Jensen RV, Stottrup NB, Kristiansen SB, Botker HE (2012) Release of a humoral circulating cardioprotective factor by remote ischemic preconditioning is dependent on preserved neural pathways in diabetic patients. Basic Res Cardiol 107:285. doi:10.1007/s00395-012-0285-1 PubMedCrossRef Jensen RV, Stottrup NB, Kristiansen SB, Botker HE (2012) Release of a humoral circulating cardioprotective factor by remote ischemic preconditioning is dependent on preserved neural pathways in diabetic patients. Basic Res Cardiol 107:285. doi:10.​1007/​s00395-012-0285-1 PubMedCrossRef
48.
49.
go back to reference Kanoria S, Jalan R, Davies NA, Seifalian AM, Williams R, Davidson BR (2006) Remote ischaemic preconditioning of the hind limb reduces experimental liver warm ischaemia-reperfusion injury. Br J Surg 93:762–768. doi:10.1002/bjs.5331 PubMedCrossRef Kanoria S, Jalan R, Davies NA, Seifalian AM, Williams R, Davidson BR (2006) Remote ischaemic preconditioning of the hind limb reduces experimental liver warm ischaemia-reperfusion injury. Br J Surg 93:762–768. doi:10.​1002/​bjs.​5331 PubMedCrossRef
50.
51.
go back to reference Karuppasamy P, Chaubey S, Dew T, Musto R, Sherwood R, Desai J, John L, Shah AM, Marber MS, Kunst G (2011) Remote intermittent ischemia before coronary artery bypass graft surgery: a strategy to reduce injury and inflammation? Basic Res Cardiol 106:511–519. doi:10.1007/s00395-011-0185-9 PubMedCrossRef Karuppasamy P, Chaubey S, Dew T, Musto R, Sherwood R, Desai J, John L, Shah AM, Marber MS, Kunst G (2011) Remote intermittent ischemia before coronary artery bypass graft surgery: a strategy to reduce injury and inflammation? Basic Res Cardiol 106:511–519. doi:10.​1007/​s00395-011-0185-9 PubMedCrossRef
52.
go back to reference Kingma JG Jr, Simard D, Voisine P, Rouleau JR (2011) Role of the autonomic nervous system in cardioprotection by remote preconditioning in isoflurane-anaesthetized dogs. Cardiovasc Res 89:384–391. doi:10.1093/cvr/cvq306 PubMedCrossRef Kingma JG Jr, Simard D, Voisine P, Rouleau JR (2011) Role of the autonomic nervous system in cardioprotection by remote preconditioning in isoflurane-anaesthetized dogs. Cardiovasc Res 89:384–391. doi:10.​1093/​cvr/​cvq306 PubMedCrossRef
53.
go back to reference Kleinbongard P, Thielmann M, Jakob H, Peters J, Heusch G, Kottenberg E (2013) Nitroglycerin does not interfere with protection by remote ischemic preconditioning in patients with surgical coronary revascularization under isoflurane anesthesia. Cardiovasc Drugs Ther 27:359–361. doi:10.1007/s10557-013-6451-3 PubMedCrossRef Kleinbongard P, Thielmann M, Jakob H, Peters J, Heusch G, Kottenberg E (2013) Nitroglycerin does not interfere with protection by remote ischemic preconditioning in patients with surgical coronary revascularization under isoflurane anesthesia. Cardiovasc Drugs Ther 27:359–361. doi:10.​1007/​s10557-013-6451-3 PubMedCrossRef
54.
go back to reference Korsheed S, Crowley LE, Fluck RJ, McIntyre CW (2013) Creation of an arteriovenous fistula is associated with significant acute local and systemic changes in microvascular function. Nephron Clin Pract 123:173–179. doi:10.1159/000353708 PubMedCrossRef Korsheed S, Crowley LE, Fluck RJ, McIntyre CW (2013) Creation of an arteriovenous fistula is associated with significant acute local and systemic changes in microvascular function. Nephron Clin Pract 123:173–179. doi:10.​1159/​000353708 PubMedCrossRef
55.
go back to reference Kottenberg E, Musiolik J, Thielmann M, Jakob H, Peters J, Heusch G (2014) Interference of propofol with signal transducer and activator of transcription 5 activation and cardioprotection by remote ischemic preconditioning during coronary artery bypass grafting. J Thorac Cardiovasc Surg 147:376–382. doi:10.1016/j.jtcvs.2013.01.005 PubMedCrossRef Kottenberg E, Musiolik J, Thielmann M, Jakob H, Peters J, Heusch G (2014) Interference of propofol with signal transducer and activator of transcription 5 activation and cardioprotection by remote ischemic preconditioning during coronary artery bypass grafting. J Thorac Cardiovasc Surg 147:376–382. doi:10.​1016/​j.​jtcvs.​2013.​01.​005 PubMedCrossRef
56.
go back to reference Kottenberg E, Thielmann M, Bergmann L, Heine T, Jakob H, Heusch G, Peters J (2012) Protection by remote ischemic preconditioning during coronary artery bypass graft surgery with isoflurane but not propofol–a clinical trial. Acta Anaesthesiol Scand 56:30–38. doi:10.1111/j.1399-6576.2011.02585.x PubMedCrossRef Kottenberg E, Thielmann M, Bergmann L, Heine T, Jakob H, Heusch G, Peters J (2012) Protection by remote ischemic preconditioning during coronary artery bypass graft surgery with isoflurane but not propofol–a clinical trial. Acta Anaesthesiol Scand 56:30–38. doi:10.​1111/​j.​1399-6576.​2011.​02585.​x PubMedCrossRef
57.
go back to reference Kottenberg E, Thielmann M, Kleinbongard P, Frey UH, Heine T, Jakob H, Heusch G, Peters J (2014) Myocardial protection by remote ischaemic pre-conditioning is abolished in sulphonylurea-treated diabetics undergoing coronary revascularisation. Acta Anaesthesiol Scand 58:453–462. doi:10.1111/aas.12278 PubMedCrossRef Kottenberg E, Thielmann M, Kleinbongard P, Frey UH, Heine T, Jakob H, Heusch G, Peters J (2014) Myocardial protection by remote ischaemic pre-conditioning is abolished in sulphonylurea-treated diabetics undergoing coronary revascularisation. Acta Anaesthesiol Scand 58:453–462. doi:10.​1111/​aas.​12278 PubMedCrossRef
58.
go back to reference Lang SC, Elsasser A, Scheler C, Vetter S, Tiefenbacher CP, Kubler W, Katus HA, Vogt AM (2006) Myocardial preconditioning and remote renal preconditioning–identifying a protective factor using proteomic methods? Basic Res Cardiol 101:149–158. doi:10.1007/s00395-005-0565-0 PubMedCrossRef Lang SC, Elsasser A, Scheler C, Vetter S, Tiefenbacher CP, Kubler W, Katus HA, Vogt AM (2006) Myocardial preconditioning and remote renal preconditioning–identifying a protective factor using proteomic methods? Basic Res Cardiol 101:149–158. doi:10.​1007/​s00395-005-0565-0 PubMedCrossRef
59.
go back to reference Lee AC, Kozuki N, Blencowe H, Vos T, Bahalim A, Darmstadt GL, Niermeyer S, Ellis M, Robertson NJ, Cousens S, Lawn JE (2013) Intrapartum-related neonatal encephalopathy incidence and impairment at regional and global levels for 2010 with trends from 1990. Pediatr Res 74(Suppl 1):50–72. doi:10.1038/pr.2013.206 PubMedCentralPubMedCrossRef Lee AC, Kozuki N, Blencowe H, Vos T, Bahalim A, Darmstadt GL, Niermeyer S, Ellis M, Robertson NJ, Cousens S, Lawn JE (2013) Intrapartum-related neonatal encephalopathy incidence and impairment at regional and global levels for 2010 with trends from 1990. Pediatr Res 74(Suppl 1):50–72. doi:10.​1038/​pr.​2013.​206 PubMedCentralPubMedCrossRef
60.
go back to reference Li J, Rohailla S, Gelber N, Rutka J, Sabah N, Gladstone RA, Wei C, Hu P, Kharbanda RK, Redington AN (2014) MicroRNA-144 is a circulating effector of remote ischemic preconditioning. Basic Res Cardiol 109:423. doi:10.1007/s00395-014-0423-z PubMedCrossRef Li J, Rohailla S, Gelber N, Rutka J, Sabah N, Gladstone RA, Wei C, Hu P, Kharbanda RK, Redington AN (2014) MicroRNA-144 is a circulating effector of remote ischemic preconditioning. Basic Res Cardiol 109:423. doi:10.​1007/​s00395-014-0423-z PubMedCrossRef
61.
go back to reference Li J, Xuan W, Yan R, Tropak MB, Jean-St-Michel E, Liang W, Gladstone R, Backx PH, Kharbanda RK, Redington AN (2011) Remote preconditioning provides potent cardioprotection via PI3K/Akt activation and is associated with nuclear accumulation of beta-catenin. Clin Sci (Lond) 120:451–462. doi:10.1042/CS20100466 CrossRef Li J, Xuan W, Yan R, Tropak MB, Jean-St-Michel E, Liang W, Gladstone R, Backx PH, Kharbanda RK, Redington AN (2011) Remote preconditioning provides potent cardioprotection via PI3K/Akt activation and is associated with nuclear accumulation of beta-catenin. Clin Sci (Lond) 120:451–462. doi:10.​1042/​CS20100466 CrossRef
62.
go back to reference Liem DA, Verdouw PD, Ploeg H, Kazim S, Duncker DJ (2002) Sites of action of adenosine in interorgan preconditioning of the heart. Am J Physiol Heart Circ Physiol 283:H29–H37PubMed Liem DA, Verdouw PD, Ploeg H, Kazim S, Duncker DJ (2002) Sites of action of adenosine in interorgan preconditioning of the heart. Am J Physiol Heart Circ Physiol 283:H29–H37PubMed
64.
go back to reference Mastitskaya S, Marina N, Gourine A, Gilbey MP, Spyer KM, Teschemacher AG, Kasparov S, Trapp S, Ackland GL, Gourine AV (2012) Cardioprotection evoked by remote ischaemic preconditioning is critically dependent on the activity of vagal pre-ganglionic neurones. Cardiovasc Res 95:487–494. doi:10.1093/cvr/cvs212 PubMedCentralPubMedCrossRef Mastitskaya S, Marina N, Gourine A, Gilbey MP, Spyer KM, Teschemacher AG, Kasparov S, Trapp S, Ackland GL, Gourine AV (2012) Cardioprotection evoked by remote ischaemic preconditioning is critically dependent on the activity of vagal pre-ganglionic neurones. Cardiovasc Res 95:487–494. doi:10.​1093/​cvr/​cvs212 PubMedCentralPubMedCrossRef
65.
go back to reference McCrindle BW, Clarizia NA, Khaikin S, Holtby HM, Manlhiot C, Schwartz SM, Caldarone CA, Coles JG, Van Arsdell GS, Scherer SW, Redington AN (2014) Remote ischemic preconditioning in children undergoing cardiac surgery with cardiopulmonary bypass: a single-center double-blinded randomized trial. J Am Heart Assoc 3(4). doi:10.1161/JAHA.114.000964 McCrindle BW, Clarizia NA, Khaikin S, Holtby HM, Manlhiot C, Schwartz SM, Caldarone CA, Coles JG, Van Arsdell GS, Scherer SW, Redington AN (2014) Remote ischemic preconditioning in children undergoing cardiac surgery with cardiopulmonary bypass: a single-center double-blinded randomized trial. J Am Heart Assoc 3(4). doi:10.​1161/​JAHA.​114.​000964
66.
go back to reference McDonald MA, Braga JR, Li J, Manlhiot C, Ross HJ, Redington AN (2014) A randomized pilot trial of remote ischemic preconditioning in heart failure with reduced ejection fraction. PLoS One 9:e105361PubMedCentralPubMedCrossRef McDonald MA, Braga JR, Li J, Manlhiot C, Ross HJ, Redington AN (2014) A randomized pilot trial of remote ischemic preconditioning in heart failure with reduced ejection fraction. PLoS One 9:e105361PubMedCentralPubMedCrossRef
67.
go back to reference Meng R, Asmaro K, Meng L, Liu Y, Ma C, Xi C, Li G, Ren C, Luo Y, Ling F, Jia J, Hua Y, Wang X, Ding Y, Lo EH, Ji X (2012) Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 79:1853–1861. doi:10.1212/WNL.0b013e318271f76a PubMedCrossRef Meng R, Asmaro K, Meng L, Liu Y, Ma C, Xi C, Li G, Ren C, Luo Y, Ling F, Jia J, Hua Y, Wang X, Ding Y, Lo EH, Ji X (2012) Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 79:1853–1861. doi:10.​1212/​WNL.​0b013e318271f76a​ PubMedCrossRef
68.
go back to reference Merlocco AC, Redington KL, Disenhouse T, Strantzas SC, Gladstone R, Wei C, Tropak MB, Manlhiot C, Li J, Redington AN (2014) Transcutaneous electrical nerve stimulation as a novel method of remote preconditioning: in vitro validation in an animal model and first human observations. Basic Res Cardiol 109:406. doi:10.1007/s00395-014-0406-0 PubMedCrossRef Merlocco AC, Redington KL, Disenhouse T, Strantzas SC, Gladstone R, Wei C, Tropak MB, Manlhiot C, Li J, Redington AN (2014) Transcutaneous electrical nerve stimulation as a novel method of remote preconditioning: in vitro validation in an animal model and first human observations. Basic Res Cardiol 109:406. doi:10.​1007/​s00395-014-0406-0 PubMedCrossRef
69.
go back to reference Meybohm P, Zacharowski K, Cremer J, Roesner J, Kletzin F, Schaelte G, Felzen M, Strouhal U, Reyher C, Heringlake M, Schon J, Brandes I, Bauer M, Knuefermann P, Wittmann M, Hachenberg T, Schilling T, Smul T, Maisch S, Sander M, Moormann T, Boening A, Weigand MA, Laufenberg R, Werner C, Winterhalter M, Treschan T, Stehr SN, Reinhart K, Hasenclever D, Brosteanu O, Bein B (2012) Remote ischaemic preconditioning for heart surgery. The study design for a multi-center randomized double-blinded controlled clinical trial–the RIPHeart-Study. Eur Heart J 33:1423–1426. doi:10.1093/eurheartj/ehs131 PubMed Meybohm P, Zacharowski K, Cremer J, Roesner J, Kletzin F, Schaelte G, Felzen M, Strouhal U, Reyher C, Heringlake M, Schon J, Brandes I, Bauer M, Knuefermann P, Wittmann M, Hachenberg T, Schilling T, Smul T, Maisch S, Sander M, Moormann T, Boening A, Weigand MA, Laufenberg R, Werner C, Winterhalter M, Treschan T, Stehr SN, Reinhart K, Hasenclever D, Brosteanu O, Bein B (2012) Remote ischaemic preconditioning for heart surgery. The study design for a multi-center randomized double-blinded controlled clinical trial–the RIPHeart-Study. Eur Heart J 33:1423–1426. doi:10.​1093/​eurheartj/​ehs131 PubMed
70.
go back to reference Moretti C, Cavallero E, D’Ascenzo F, Cerrato E, Zoccai GB, Omede P, Presutti DG, Lefevre T, Sanguineti F, Picchi A, Palazzuoli A, Carini G, Giammaria M, Ugo F, Presbitero P, Chen S, Lin S, Sheiban I, Gaita F (2014) The EUROpean and Chinese cardiac and renal Remote Ischemic Preconditioning Study (EURO-CRIPS): study design and methods. J Cardiovasc Med (Hagerstown). doi:10.2459/JCM.0000000000000098 (Epub ahead of print) Moretti C, Cavallero E, D’Ascenzo F, Cerrato E, Zoccai GB, Omede P, Presutti DG, Lefevre T, Sanguineti F, Picchi A, Palazzuoli A, Carini G, Giammaria M, Ugo F, Presbitero P, Chen S, Lin S, Sheiban I, Gaita F (2014) The EUROpean and Chinese cardiac and renal Remote Ischemic Preconditioning Study (EURO-CRIPS): study design and methods. J Cardiovasc Med (Hagerstown). doi:10.​2459/​JCM.​0000000000000098​ (Epub ahead of print)
72.
go back to reference Ovize M, Baxter GF, Di Lisa F, Ferdinandy P, Garcia-Dorado D, Hausenloy DJ, Heusch G, Vinten-Johansen J, Yellon DM, Schulz R (2010) Postconditioning and protection from reperfusion injury: where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res 87:406–423. doi:10.1093/cvr/cvq129 PubMedCrossRef Ovize M, Baxter GF, Di Lisa F, Ferdinandy P, Garcia-Dorado D, Hausenloy DJ, Heusch G, Vinten-Johansen J, Yellon DM, Schulz R (2010) Postconditioning and protection from reperfusion injury: where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res 87:406–423. doi:10.​1093/​cvr/​cvq129 PubMedCrossRef
73.
75.
go back to reference Prunier F, Angoulvant D, Saint EC, Vermes E, Gilard M, Piot C, Roubille F, Elbaz M, Ovize M, Biere L, Jeanneteau J, Delepine S, Benard T, Abi-Khalil W, Furber A (2014) The RIPOST-MI study, assessing remote ischemic perconditioning alone or in combination with local ischemic postconditioning in ST-segment elevation myocardial infarction. Basic Res Cardiol 109:400. doi:10.1007/s00395-013-0400-y PubMedCrossRef Prunier F, Angoulvant D, Saint EC, Vermes E, Gilard M, Piot C, Roubille F, Elbaz M, Ovize M, Biere L, Jeanneteau J, Delepine S, Benard T, Abi-Khalil W, Furber A (2014) The RIPOST-MI study, assessing remote ischemic perconditioning alone or in combination with local ischemic postconditioning in ST-segment elevation myocardial infarction. Basic Res Cardiol 109:400. doi:10.​1007/​s00395-013-0400-y PubMedCrossRef
77.
go back to reference Rahman IA, Mascaro JG, Steeds RP, Frenneaux MP, Nightingale P, Gosling P, Townsend P, Townend JN, Green D, Bonser RS (2010) Remote ischemic preconditioning in human coronary artery bypass surgery: from promise to disappointment? Circulation 122:S53–S59. doi:10.1161/CIRCULATIONAHA PubMedCrossRef Rahman IA, Mascaro JG, Steeds RP, Frenneaux MP, Nightingale P, Gosling P, Townsend P, Townend JN, Green D, Bonser RS (2010) Remote ischemic preconditioning in human coronary artery bypass surgery: from promise to disappointment? Circulation 122:S53–S59. doi:10.​1161/​CIRCULATIONAHA PubMedCrossRef
80.
go back to reference Redington KL, Disenhouse T, Li J, Wei C, Dai X, Gladstone R, Manlhiot C, Redington AN (2013) Electroacupuncture reduces myocardial infarct size and improves post-ischemic recovery by invoking release of humoral, dialyzable, cardioprotective factors. J Physiol Sci 63:219–223. doi:10.1007/s12576-013-0259-6 PubMedCrossRef Redington KL, Disenhouse T, Li J, Wei C, Dai X, Gladstone R, Manlhiot C, Redington AN (2013) Electroacupuncture reduces myocardial infarct size and improves post-ischemic recovery by invoking release of humoral, dialyzable, cardioprotective factors. J Physiol Sci 63:219–223. doi:10.​1007/​s12576-013-0259-6 PubMedCrossRef
81.
go back to reference Redington KL, Disenhouse T, Strantzas SC, Gladstone R, Wei C, Tropak MB, Dai X, Manlhiot C, Li J, Redington AN (2012) Remote cardioprotection by direct peripheral nerve stimulation and topical capsaicin is mediated by circulating humoral factors. Basic Res Cardiol 107:241. doi:10.1007/s00395-011-0241-5 PubMedCrossRef Redington KL, Disenhouse T, Strantzas SC, Gladstone R, Wei C, Tropak MB, Dai X, Manlhiot C, Li J, Redington AN (2012) Remote cardioprotection by direct peripheral nerve stimulation and topical capsaicin is mediated by circulating humoral factors. Basic Res Cardiol 107:241. doi:10.​1007/​s00395-011-0241-5 PubMedCrossRef
82.
go back to reference Rentoukas I, Giannopoulos G, Kaoukis A, Kossyvakis C, Raisakis K, Driva M, Panagopoulou V, Tsarouchas K, Vavetsi S, Pyrgakis V, Deftereos S (2010) Cardioprotective role of remote ischemic periconditioning in primary percutaneous coronary intervention: enhancement by opioid action. JACC Cardiovasc Interv 3:49–55. doi:10.1016/j.jcin.2009.10.015 PubMedCrossRef Rentoukas I, Giannopoulos G, Kaoukis A, Kossyvakis C, Raisakis K, Driva M, Panagopoulou V, Tsarouchas K, Vavetsi S, Pyrgakis V, Deftereos S (2010) Cardioprotective role of remote ischemic periconditioning in primary percutaneous coronary intervention: enhancement by opioid action. JACC Cardiovasc Interv 3:49–55. doi:10.​1016/​j.​jcin.​2009.​10.​015 PubMedCrossRef
83.
go back to reference Schwartz LL, Kloner RA, Arai AE, Baines CP, Bolli R, Braunwald E, Downey J, Gibbons RJ, Gottlieb RA, Heusch G, Jennings RB, Lefer DJ, Mentzer RM, Murphy E, Ovize M, Ping P, Przyklenk K, Sack MN, Vander Heide RS, Vinten-Johansen J, Yellon DM (2011) New horizons in cardioprotection: recommendations from the 2010 national heart, lung, and blood institute workshop. Circulation 124:1172–1179. doi:10.1161/CIRCULATIONAHA.111.032698 CrossRef Schwartz LL, Kloner RA, Arai AE, Baines CP, Bolli R, Braunwald E, Downey J, Gibbons RJ, Gottlieb RA, Heusch G, Jennings RB, Lefer DJ, Mentzer RM, Murphy E, Ovize M, Ping P, Przyklenk K, Sack MN, Vander Heide RS, Vinten-Johansen J, Yellon DM (2011) New horizons in cardioprotection: recommendations from the 2010 national heart, lung, and blood institute workshop. Circulation 124:1172–1179. doi:10.​1161/​CIRCULATIONAHA.​111.​032698 CrossRef
84.
go back to reference Shimizu M, Tropak M, Diaz RJ, Suto F, Surendra H, Kuzmin E, Li J, Gross G, Wilson GJ, Callahan J, Redington AN (2009) Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: evidence suggesting cross-species protection. Clin Sci (Lond) 117:191–200. doi:10.1042/CS20080523 CrossRef Shimizu M, Tropak M, Diaz RJ, Suto F, Surendra H, Kuzmin E, Li J, Gross G, Wilson GJ, Callahan J, Redington AN (2009) Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: evidence suggesting cross-species protection. Clin Sci (Lond) 117:191–200. doi:10.​1042/​CS20080523 CrossRef
85.
go back to reference Sloth AD, Schmidt MR, Munk K, Kharbanda RK, Redington AN, Schmidt M, Pedersen L, Sorensen HT, Botker HE (2014) Improved long-term clinical outcomes in patients with ST-elevation myocardial infarction undergoing remote ischaemic conditioning as an adjunct to primary percutaneous coronary intervention. Eur Heart J 35:168–175. doi:10.1093/eurheartj/eht369 PubMedCrossRef Sloth AD, Schmidt MR, Munk K, Kharbanda RK, Redington AN, Schmidt M, Pedersen L, Sorensen HT, Botker HE (2014) Improved long-term clinical outcomes in patients with ST-elevation myocardial infarction undergoing remote ischaemic conditioning as an adjunct to primary percutaneous coronary intervention. Eur Heart J 35:168–175. doi:10.​1093/​eurheartj/​eht369 PubMedCrossRef
86.
go back to reference Steensrud T, Li J, Dai X, Manlhiot C, Kharbanda RK, Tropak M, Redington A (2010) Pretreatment with the nitric oxide donor SNAP or nerve transection blocks humoral preconditioning by remote limb ischemia or intra-arterial adenosine. Am J Physiol Heart Circ Physiol 299:H1598–H1603. doi:10.1152/ajpheart.00396.2010 PubMedCrossRef Steensrud T, Li J, Dai X, Manlhiot C, Kharbanda RK, Tropak M, Redington A (2010) Pretreatment with the nitric oxide donor SNAP or nerve transection blocks humoral preconditioning by remote limb ischemia or intra-arterial adenosine. Am J Physiol Heart Circ Physiol 299:H1598–H1603. doi:10.​1152/​ajpheart.​00396.​2010 PubMedCrossRef
87.
go back to reference Tang ZL, Dai W, Li YJ, Deng HW (1999) Involvement of capsaicin-sensitive sensory nerves in early and delayed cardioprotection induced by a brief ischaemia of the small intestine. Naunyn Schmiedebergs Arch Pharmacol 359:243–247. doi:10.1007/PL00005348 PubMedCrossRef Tang ZL, Dai W, Li YJ, Deng HW (1999) Involvement of capsaicin-sensitive sensory nerves in early and delayed cardioprotection induced by a brief ischaemia of the small intestine. Naunyn Schmiedebergs Arch Pharmacol 359:243–247. doi:10.​1007/​PL00005348 PubMedCrossRef
89.
go back to reference Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, Peters J, Jakob H, Heusch G (2010) Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass surgery with crystalloid cardioplegic arrest. Basic Res Cardiol 105:657–664. doi:10.1007/s00395-010-0104-5 PubMedCrossRef Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, Peters J, Jakob H, Heusch G (2010) Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass surgery with crystalloid cardioplegic arrest. Basic Res Cardiol 105:657–664. doi:10.​1007/​s00395-010-0104-5 PubMedCrossRef
90.
go back to reference Thielmann M, Kottenberg E, Kleinbongard P, Wendt D, Gedik N, Pasa S, Price V, Tsagakis K, Neuhauser M, Peters J, Jakob H, Heusch G (2013) Cardioprotective and prognostic effects of remote ischaemic preconditioning in patients undergoing coronary artery bypass surgery: a single-centre randomised, double-blind, controlled trial. Lancet 382:597–604. doi:10.1016/S0140-6736(13)61450-6 PubMedCrossRef Thielmann M, Kottenberg E, Kleinbongard P, Wendt D, Gedik N, Pasa S, Price V, Tsagakis K, Neuhauser M, Peters J, Jakob H, Heusch G (2013) Cardioprotective and prognostic effects of remote ischaemic preconditioning in patients undergoing coronary artery bypass surgery: a single-centre randomised, double-blind, controlled trial. Lancet 382:597–604. doi:10.​1016/​S0140-6736(13)61450-6 PubMedCrossRef
91.
92.
go back to reference Walsh SR, Boyle JR, Tang TY, Sadat U, Cooper DG, Lapsley M, Norden AG, Varty K, Hayes PD, Gaunt ME (2009) Remote ischemic preconditioning for renal and cardiac protection during endovascular aneurysm repair: a randomized controlled trial. J Endovasc Ther 16:680–689. doi:10.1583/09-2817.1 PubMedCrossRef Walsh SR, Boyle JR, Tang TY, Sadat U, Cooper DG, Lapsley M, Norden AG, Varty K, Hayes PD, Gaunt ME (2009) Remote ischemic preconditioning for renal and cardiac protection during endovascular aneurysm repair: a randomized controlled trial. J Endovasc Ther 16:680–689. doi:10.​1583/​09-2817.​1 PubMedCrossRef
93.
go back to reference Wei M, Xin P, Li S, Tao J, Li Y, Li J, Liu M, Li J, Zhu W, Redington AN (2011) Repeated remote ischemic postconditioning protects against adverse left ventricular remodeling and improves survival in a rat model of myocardial infarction. Circ Res 108:1220–1225. doi:10.1161/CIRCRESAHA.110.236190 PubMedCrossRef Wei M, Xin P, Li S, Tao J, Li Y, Li J, Liu M, Li J, Zhu W, Redington AN (2011) Repeated remote ischemic postconditioning protects against adverse left ventricular remodeling and improves survival in a rat model of myocardial infarction. Circ Res 108:1220–1225. doi:10.​1161/​CIRCRESAHA.​110.​236190 PubMedCrossRef
94.
go back to reference White SK, Frohlich GM, Sado DM, Maestrini V, Fontana M, Treibel TA, Tehrani S, Flett AS, Meier P, Ariti C, Davies JR, Moon JC, Yellon DM, Hausenloy DJ (2014) Remote ischemic conditioning reduces myocardial infarct size and edema in patients with st-segment elevation myocardial infarction. JACC Cardiovasc Interv. doi:10.1016/j.jcin.2014.05.015 (Epub ahead of print) White SK, Frohlich GM, Sado DM, Maestrini V, Fontana M, Treibel TA, Tehrani S, Flett AS, Meier P, Ariti C, Davies JR, Moon JC, Yellon DM, Hausenloy DJ (2014) Remote ischemic conditioning reduces myocardial infarct size and edema in patients with st-segment elevation myocardial infarction. JACC Cardiovasc Interv. doi:10.​1016/​j.​jcin.​2014.​05.​015 (Epub ahead of print)
Metadata
Title
Remote ischemic conditioning: from experimental observation to clinical application: report from the 8th Biennial Hatter Cardiovascular Institute Workshop
Authors
Jack M. J. Pickard
Hans Erik Bøtker
Gabriele Crimi
Brian Davidson
Sean M. Davidson
David Dutka
Peter Ferdinandy
Rocky Ganske
David Garcia-Dorado
Zoltan Giricz
Alexander V. Gourine
Gerd Heusch
Rajesh Kharbanda
Petra Kleinbongard
Raymond MacAllister
Christopher McIntyre
Patrick Meybohm
Fabrice Prunier
Andrew Redington
Nicola J. Robertson
M. Saadeh Suleiman
Andrew Vanezis
Stewart Walsh
Derek M. Yellon
Derek J. Hausenloy
Publication date
01-01-2015
Publisher
Springer Berlin Heidelberg
Published in
Basic Research in Cardiology / Issue 1/2015
Print ISSN: 0300-8428
Electronic ISSN: 1435-1803
DOI
https://doi.org/10.1007/s00395-014-0453-6

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