Remote ischemic conditioning: Current clinical perspectives

Journal of Cardiology

Volumn 66, Issue 2, 2015, Pages 91-96

  Le Page, Sophie ^a   Prunier, Fabrice ^a  

^a UNIVERSITÉ D'ANGERS   (France)

Author keywords

Cardioprotection; Conditioning; Ischemia reperfusion injury

Indexed keywords

CARDIOVASCULAR PROCEDURE; CORONARY ARTERY BYPASS SURGERY; HEART MUSCLE INJURY; HUMAN; NEUROPROTECTION; ORGAN TRANSPLANTATION; PEDIATRIC SURGERY; PERCUTANEOUS CORONARY INTERVENTION; REMOTE ISCHEMIC CONDITIONING; RENAL PROTECTION; REVIEW; SOLID ORGAN TRANSPLANTATION; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; VASCULAR SURGERY; CORONARY ARTERY BYPASS GRAFT; HEART INFARCTION PREVENTION; MYOCARDIAL REPERFUSION INJURY;

CORONARY ARTERY BYPASS; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MYOCARDIAL REPERFUSION INJURY; PERCUTANEOUS CORONARY INTERVENTION;

EID: 84932199367     PISSN: 09145087     EISSN: 18764738     Source Type: Journal    
DOI: 10.1016/j.jjcc.2015.01.009     Document Type: Review

References (61)

1. Jennings R.B., Sommers H.M., Smyth G.A., Flack H.A., Linn H. Myocardial necrosis induced by temporary occlusion of a coronary artery in the dog. Arch Pathol 1960, 70:68-78.
2. Murry C.E., Jennings R.B., Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986, 74:1124-1136.
3. Zhao Z.Q., Corvera J.S., Halkos M.E., Kerendi F., Wang N.P., Guyton R.A., Vinten-Johansen J. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 2003, 285:H579-H588.
4. Staat P., Rioufol G., Piot C., Cottin Y., Cung T.T., L'Huillier I., Aupetit J.F., Bonnefoy E., Finet G., André-Fouët X., Ovize M. Postconditioning the human heart. Circulation 2005, 112:2143-2148.
5. Ovize M., Mewton N. Interventional cardiology: ischaemic POSTconditioning - a long harvest for a little corn. Nat Rev Cardiol 2014, 11:8-10.
6. Przyklenk K., Bauer B., Ovize M., Kloner R.A., Whittaker P. Regional ischemic 'preconditioning' protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation 1993, 87:893-899.
7. Heusch G. Cardioprotection: chances and challenges of its translation to the clinic. Lancet 2013, 381:166-175.
8. Gunaydin B., Cakici I., Soncul H., Kalaycioglu S., Cevik C., Sancak B., Kanzik I., Karadenizli Y. Does remote organ ischaemia trigger cardiac preconditioning during coronary artery surgery?. Pharmacol Res 2000, 41:493-496.
9. Cheung M.M., Kharbanda R.K., Konstantinov I.E., Shimizu M., Frndova H., Li J., Holtby H.M., Cox P.N., Smallhorn J.F., Van Arsdell G.S., Redington A.N. Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol 2006, 47:2277-2282.
10. Hausenloy D.J., Mwamure P.K., Venugopal V., Harris J., Barnard M., Grundy E., Ashley E., Vichare S., Di Salvo C., Kolvekar S., Hayward M., Keogh B., MacAllister R.J., Yellon D.M. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet 2007, 370:575-579.
11. Yetgin T., Manintveld O.C., Boersma E., Kappetein A.P., van Geuns R.J., Zijlstra F., Duncker D.J., van der Giessen W.J. Remote ischemic conditioning in percutaneous coronary intervention and coronary artery bypass grafting. Circ J 2012, 76:2392-2404.
12. Zhang B., Zhou J., Li H., Zhou M., Chen A., Zhao Q. Remote ischemic preconditioning does not improve the clinical outcomes in patients undergoing coronary artery bypass grafting: a meta-analysis of randomized controlled trials. Int J Cardiol 2014, 172:e36-e38.
13. Thielmann M., Kottenberg E., Kleinbongard P., Wendt D., Gedik N., Pasa S., Price V., Tsagakis K., Neuhäuser M., Peters J., Jakob H., Heusch G. Cardioprotective and prognostic effects of remote ischaemic preconditioning in patients undergoing coronary artery bypass surgery: a single-centre randomised, double-blind, controlled trial. Lancet 2013, 382:597-604.
14. Hong D.M., Lee E.H., Kim H.J., Min J.J., Chin J.H., Choi D.K., Bahk J.H., Sim J.Y., Choi I.C., Jeon Y. Does remote ischaemic preconditioning with postconditioning improve clinical outcomes of patients undergoing cardiac surgery? Remote Ischaemic Preconditioning with Postconditioning Outcome Trial. Eur Heart J 2014, 35:176-183.
15. Young P.J., Dalley P., Garden A., Horrocks C., La Flamme A., Mahon B., Miller J., Pilcher J., Weatherall M., Williams J., Young W., Beasley R. A pilot study investigating the effects of remote ischemic preconditioning in high-risk cardiac surgery using a randomised controlled double-blind protocol. Basic Res Cardiol 2012, 107:256.
16. Rentoukas I., Giannopoulos G., Kaoukis A., Kossyvakis C., Raisakis K., Driva M., Panagopoulou V., Tsarouchas K., Vavetsi S., Pyrgakis V., Deftereos S. Cardioprotective role of remote ischemic periconditioning in primary percutaneous coronary intervention: enhancement by opioid action. JACC Cardiovasc Interv 2010, 3:49-55.
17. Botker H.E., Kharbanda R., Schmidt M.R., Bottcher M., Kaltoft A.K., Terkelsen C.J., Munk K., Andersen N.H., Hansen T.M., Trautner S., Lassen J.F., Christiansen E.H., Krusell L.R., Kristensen S.D., Thuesen L., et al. 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 2010, 375:727-734.
18. Crimi G., Pica S., Raineri C., Bramucci E., De Ferrari G.M., Klersy C., Ferlini M., Marinoni B., Repetto A., Romeo M., Rosti V., Massa M., Raisaro A., Leonardi S., Rubartelli P., et al. 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 2013, 6:1055-1063.
19. Prunier F., Angoulvant D., Saint Etienne C., Vermes E., Gilard M., Piot C., Roubille F., Elbaz M., Ovize M., Bière L., Jeanneteau J., Delépine S., Benard T., Abi-Khalil W., Furber A. 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 2014, 109:400.
20. White S.K., Frohlich G.M., Sado D.M., Maestrini V., Fontana M., Treibel T.A., Tehrani S., Flett A.S., Meier P., Ariti C., Davies J.R., Moon J.C., Yellon D.M., Hausenloy D.J. Remote ischemic conditioning reduces myocardial infarct size and edema in patients with ST-segment elevation myocardial infarction. JACC Cardiovasc Interv 2015, 8(1PB):178-188.
21. Hoole S.P., Heck P.M., Sharples L., Khan S.N., Duehmke R., Densem C.G., Clarke S.C., Shapiro L.M., Schofield P.M., O'Sullivan M., Dutka D.P. Cardiac Remote Ischemic Preconditioning in Coronary Stenting (CRISP Stent) Study: a prospective, randomized control trial. Circulation 2009, 119:820-827.
22. Davies W.R., Brown A.J., Watson W., McCormick L.M., West N.E., Dutka D.P., Hoole S.P. Remote ischemic preconditioning improves outcome at 6 years after elective percutaneous coronary intervention: the CRISP stent trial long-term follow-up. Circ Cardiovasc Interv 2013, 6:246-251.
23. Carrasco-Chinchilla F., Munoz-Garcia A.J., Dominguez-Franco A., Millan-Vazquez G., Guerrero-Molina A., Ortiz-Garcia C., Enguix-Armada A., Alonso-Briales J.H., Hernández-García J.M., de Teresa-Galván E., Jiménez-Navarro M.F. Remote ischaemic postconditioning: does it protect against ischaemic damage in percutaneous coronary revascularisation? Randomised placebo-controlled clinical trial. Heart 2013, 99:1431-1437.
24. Lavi S., D'Alfonso S., Diamantouros P., Camuglia A., Garg P., Teefy P., Jablonsky G., Sridhar K., Lavi R. Remote ischemic postconditioning during percutaneous coronary interventions: remote ischemic postconditioning-percutaneous coronary intervention randomized trial. Circ Cardiovasc Interv 2014, 7:225-232.
25. Ali Z.A., Callaghan C.J., Lim E., Ali A.A., Nouraei S.A., Akthar A.M., Boyle J.R., Varty K., Kharbanda R.K., Dutka D.P., Gaunt M.E. Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial. Circulation 2007, 116:I98-I105.
26. Li C., Li Y.S., Xu M., Wen S.H., Yao X., Wu Y., Huang C.Y., Huang W.Q., Liu K.X. Limb remote ischemic preconditioning for intestinal and pulmonary protection during elective open infrarenal abdominal aortic aneurysm repair: a randomized controlled trial. Anesthesiology 2013, 118:842-852.
27. Walsh S.R., Nouraei S.A., Tang T.Y., Sadat U., Carpenter R.H., Gaunt M.E. Remote ischemic preconditioning for cerebral and cardiac protection during carotid endarterectomy: results from a pilot randomized clinical trial. Vasc Endovascular Surg 2010, 44:434-439.
28. Walsh S.R., Sadat U., Boyle J.R., Tang T.Y., Lapsley M., Norden A.G., Gaunt M.E. Remote ischemic preconditioning for renal protection during elective open infrarenal abdominal aortic aneurysm repair: randomized controlled trial. Vasc Endovascular Surg 2010, 44:334-340.
29. Walsh S.R., Boyle J.R., Tang T.Y., Sadat U., Cooper D.G., Lapsley M., Norden A.G., Varty K., Hayes P.D., Gaunt M.E. Remote ischemic preconditioning for renal and cardiac protection during endovascular aneurysm repair: a randomized controlled trial. J Endovasc Ther 2009, 16:680-689.
30. Murphy N., Vijayan A., Frohlich S., O'Farrell F., Barry M., Sheehan S., Boylan J., Conlon N. Remote ischemic preconditioning does not affect the incidence of acute kidney injury after elective abdominal aortic aneurysm repair. J Cardiothorac Vasc Anesth 2014, 28:1285-1292.
31. Desai M., Gurusamy K.S., Ghanbari H., Hamilton G., Seifalian A.M. Remote ischaemic preconditioning versus no remote ischaemic preconditioning for vascular and endovascular surgical procedures. Cochrane Database Syst Rev 2011, CD008472.
32. Zimmerman R.F., Ezeanuna P.U., Kane J.C., Cleland C.D., Kempananjappa T.J., Lucas F.L., Kramer R.S. Ischemic preconditioning at a remote site prevents acute kidney injury in patients following cardiac surgery. Kidney Int 2011, 80:861-867.
33. Deftereos S., Giannopoulos G., Tzalamouras V., Raisakis K., Kossyvakis C., Kaoukis A., Panagopoulou V., Karageorgiou S., Avramides D., Toutouzas K., Hahalis G., Pyrgakis V., Manolis A.S., Alexopoulos D., Stefanadis C., et al. Renoprotective effect of remote ischemic post-conditioning by intermittent balloon inflations in patients undergoing percutaneous coronary intervention. J Am Coll Cardiol 2013, 61:1949-1955.
34. Er F., Nia A.M., Dopp H., Hellmich M., Dahlem K.M., Caglayan E., Kubacki T., Benzing T., Erdmann E., Burst V., Gassanov N. Ischemic preconditioning for prevention of contrast medium-induced nephropathy: randomized pilot RenPro Trial (Renal Protection Trial). Circulation 2012, 126:296-303.
35. Igarashi G., Iino K., Watanabe H., Ito H. Remote ischemic pre-conditioning alleviates contrast-induced acute kidney injury in patients with moderate chronic kidney disease. Circ J 2013, 77:3037-3044.
36. Huang J., Chen Y., Dong B., Kong W., Zhang J., Xue W., Liu D., Huang Y. Effect of remote ischaemic preconditioning on renal protection in patients undergoing laparoscopic partial nephrectomy: a 'blinded' randomised controlled trial. BJU Int 2013, 112:74-80.
37. Yang Y., Lang X.B., Zhang P., Lv R., Wang Y.F., Chen J.H. Remote ischemic preconditioning for prevention of acute kidney injury: a meta-analysis of randomized controlled trials. Am J Kidney Dis 2014, 64:574-583.
38. Gonzalez N.R., Connolly M., Dusick J.R., Bhakta H., Vespa P. Phase I clinical trial for the feasibility and safety of remote ischemic conditioning for aneurysmal subarachnoid hemorrhage. Neurosurgery 2014, 75:590-598.
39. Koch S., Katsnelson M., Dong C., Perez-Pinzon M. Remote ischemic limb preconditioning after subarachnoid hemorrhage: a phase Ib study of safety and feasibility. Stroke 2011, 42:1387-1391.
40. Hu S., Dong H.L., Li Y.Z., Luo Z.J., Sun L., Yang Q.Z., Yang L.F., Xiong L. Effects of remote ischemic preconditioning on biochemical markers and neurologic outcomes in patients undergoing elective cervical decompression surgery: a prospective randomized controlled trial. J Neurosurg Anaesthesiol 2010, 22:46-52.
41. Hougaard K.D., Hjort N., Zeidler D., Sorensen L., Norgaard A., Hansen T.M., von Weitzel-Mudersbach P., Simonsen C.Z., Damgaard D., Gottrup H., Svendsen K., Rasmussen P.V., Ribe L.R., Mikkelsen I.K., Nagenthiraja K., et al. Remote ischemic perconditioning as an adjunct therapy to thrombolysis in patients with acute ischemic stroke: a randomized trial. Stroke 2014, 45:159-167.
42. 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 E.H., et al. Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 2012, 79:1853-1861.
43. Chen Y., Zheng H., Wang X., Zhou Z., Luo A., Tian Y. Remote ischemic preconditioning fails to improve early renal function of patients undergoing living-donor renal transplantation: a randomized controlled trial. Transplantation 2013, 95:e4-e6.
44. Wu J., Feng X., Huang H., Shou Z., Zhang X., Wang R., Chen Y., Chen J. Remote ischemic conditioning enhanced the early recovery of renal function in recipients after kidney transplantation: a randomized controlled trial. J Surg Res 2014, 188:303-308.
45. Lin E., Snell G.I., Levvey B.J., Mifsud N., Paul M., Buckland M.R., Gooi J., Marasco S., Sharland A.F., Myles P.S. Safety, feasibility, and effect of remote ischemic conditioning in patients undergoing lung transplantation. J Heart Lung Transplant 2014, 33:1139-1148.
46. Hausenloy D.J., Yellon D.M. Remote ischaemic preconditioning: underlying mechanisms and clinical application. Cardiovasc Res 2008, 79:377-386.
47. Breivik L., Helgeland E., Aarnes E.K., Mrdalj J., Jonassen A.K. Remote postconditioning by humoral factors in effluent from ischemic preconditioned rat hearts is mediated via PI3K/Akt-dependent cell-survival signaling at reperfusion. Basic Res Cardiol 2011, 106:135-145.
48. Lim S.Y., Yellon D.M., Hausenloy D.J. The neural and humoral pathways in remote limb ischemic preconditioning. Basic Res Cardiol 2010, 105:651-655.
49. Shimizu M., Saxena P., Konstantinov I.E., Cherepanov V., Cheung M.M., Wearden P., Zhangdong H., Schmidt M., Downey G.P., Redington A.N. Remote ischemic preconditioning decreases adhesion and selectively modifies functional responses of human neutrophils. J Surg Res 2010, 158:155-161.
50. Wolfrum S., Schneider K., Heidbreder M., Nienstedt J., Dominiak P., Dendorfer A. Remote preconditioning protects the heart by activating myocardial PKCepsilon-isoform. Cardiovasc Res 2002, 55:583-589.
51. Weinbrenner C., Schulze F., Sarvary L., Strasser R.H. Remote preconditioning by infrarenal aortic occlusion is operative via delta1-opioid receptors and free radicals in vivo in the rat heart. Cardiovasc Res 2004, 61:591-599.
52. Kerendi F., Kin H., Halkos M.E., Jiang R., Zatta A.J., Zhao Z.Q., Guyton R.A., Vinten-Johansen J. Remote postconditioning. Brief renal ischemia and reperfusion applied before coronary artery reperfusion reduces myocardial infarct size via endogenous activation of adenosine receptors. Basic Res Cardiol 2005, 100:404-412.
53. Diwan V., Jaggi A.S., Singh M., Singh N., Singh D. Possible involvement of erythropoietin in remote renal preconditioning-induced cardioprotection in rats. J Cardiovasc Pharmacol 2008, 51:126-130.
54. Hajrasouliha A.R., Tavakoli S., Ghasemi M., Jabehdar-Maralani P., Sadeghipour H., Ebrahimi F., Dehpour A.R. Endogenous cannabinoids contribute to remote ischemic preconditioning via cannabinoid CB2 receptors in the rat heart. Eur J Pharmacol 2008, 579:246-252.
55. Giricz Z., Varga Z.V., Baranyai T., Sipos P., Paloczi K., Kittel A., Buzás E.I., Ferdinandy P. Cardioprotection by remote ischemic preconditioning of the rat heart is mediated by extracellular vesicles. J Mol Cell Cardiol 2014, 68:75-78.
56. Hibert P., Prunier-Mirebeau D., Beseme O., Chwastyniak M., Tamareille S., Lamon D., Furber A., Pinet F., Prunier F. Apolipoprotein a-I is a potential mediator of remote ischemic preconditioning. PLoS One 2013, 8:e77211.
57. Li J., Rohailla S., Gelber N., Rutka J., Sabah N., Gladstone R.A., Wei C., Hu P., Kharbanda R.K., Redington A.N. MicroRNA-144 is a circulating effector of remote ischemic preconditioning. Basic Res Cardiol 2014, 109:423.
58. Ghaemian A., Nouraei S.M., Abdollahian F., Naghshvar F., Giussani D.A., Nouraei S.A. Remote ischemic preconditioning in percutaneous coronary revascularization: a double-blind randomized controlled clinical trial. Asian Cardiovasc Thorac Ann 2012, 20:548-554.
59. Candilio L., Malik A., Ariti C., Barnard M., Di Salvo C., Lawrence D., Hayward M., Yap J., Roberts N., Sheikh A., Kolvekar S., Hausenloy D.J., Yellon D.M. Effect of remote ischaemic preconditioning on clinical outcomes in patients undergoing cardiac bypass surgery: a randomised controlled clinical trial. Heart 2015, 101:185-192.
60. Sloth A.D., Schmidt M.R., Munk K., Kharbanda R.K., Redington A.N., Schmidt M., Pedersen L., Sørensen H.T., Bøtker H.E., CONDI Investigators 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 2014, 35:168-175.
61. Remote Preconditioning Trialists' Group, Healy D.A., Khan W.A., Wong C.S., Moloney M.C., Grace P.A., Coffey J.C., Dunne C., Walsh S.R., Sadat U., Gaunt M.E., Chen S., Tehrani S., Hausenloy D.J., Yellon D.M., et al. Remote preconditioning and major clinical complications following adult cardiovascular surgery: systematic review and meta-analysis. Int J Cardiol 2014, 176:20-31.