Remote ischaemic conditioning reduces infarct size in animal in vivo models of ischaemia-reperfusion injury: A systematic review and meta-analysis

Cardiovascular Research

Volumn 113, Issue 3, 2017, Pages 288-297

  Bromage, Daniel I ^a   Pickard, Jack M J ^a   Rossello, Xavier ^a   Ziff, Oliver J ^a   Burke, Niall ^a   Yellon, Derek M ^a   Davidson, Sean M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Infarct size; Ischaemia; Meta analysis; Preconditioning; Reperfusion

Indexed keywords

ANIMAL; CARDIAC MUSCLE; DISEASE MODEL; ISCHEMIC PRECONDITIONING; META ANALYSIS; METABOLISM; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; PATHOLOGY; PROCEDURES; REPRODUCIBILITY;

ANIMALS; DISEASE MODELS, ANIMAL; ISCHEMIC PRECONDITIONING; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; REPRODUCIBILITY OF RESULTS;

EID: 85030615767     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvw219     Document Type: Review

References (74)

1. Pedersen F, Butrymovich V, Kelbaek H, Wachtell K, Helqvist S, Kastrup J, Holmvang L, Clemmensen P, Engstrom T, Grande P, Saunamaki K, Jorgensen E. Short- A nd longterm cause of death in patients treated with primary PCI for STEMI. J Am Coll Cardiol 2014;64:2101-2108.
2. Birnbaum Y, Hale SL, Kloner RA. Ischemic preconditioning at a distance: Reduction of myocardial infarct size by partial reduction of blood supply combined with rapid stimulation of the gastrocnemius muscle in the rabbit. Circulation 1997;96:1641-1646.
3. 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.
4. 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. 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.
5. Venugopal V, Hausenloy DJ, Ludman A, Di Salvo C, Kolvekar S, Yap J, Lawrence D, Bognolo J, Yellon DM. Remote ischaemic preconditioning reduces myocardial injury in patients undergoing cardiac surgery with cold-blood cardioplegia: A randomised controlled trial. Heart 2009;95:1567-1571.
6. Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, Peters J, Jakob H, Heusch G. Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass surgery with crystalloid cardioplegic arrest. Basic Res Cardiol 2010;105:657-664.
7. Ali ZA, Callaghan CJ, Lim E, Ali AA, Nouraei SA, Akthar AM, Boyle JR, Varty K, Kharbanda RK, Dutka DP, Gaunt ME. Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: A randomized controlled trial. Circulation 2007;116:I98-105.
8. Walsh SR, Boyle JR, Tang TY, Sadat U, Cooper DG, Lapsley M, Norden AG, Varty K, Hayes PD, Gaunt ME. Remote ischemic preconditioning for renal and cardiac protection during endovascular aneurysm repair: A randomized controlled trial. J Endovasc Ther 2009;16:680-689.
9. Hu S, Dong HL, Li YZ, Luo ZJ, Sun L, Yang QZ, Yang LF, 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 Anesthesiol 2010;22:46-52.
10. Hoole SP, Heck PM, Sharples L, Khan SN, Duehmke R, Densem CG, Clarke SC, Shapiro LM, Schofield PM, O'Sullivan M, Dutka DP. Cardiac Remote Ischemic Preconditioning in Coronary Stenting (CRISP Stent) study: A prospective, randomized control trial. Circulation 2009;119:820-827.
11. 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. 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.
12. Schmidt MR, Smerup M, Konstantinov IE, Shimizu M, Li J, Cheung M, White PA, Kristiansen SB, Sorensen K, Dzavik V, Redington AN, Kharbanda RK. Intermittent peripheral tissue ischemia during coronary ischemia reduces myocardial infarction through a KATP-dependent mechanism: First demonstration of remote ischemic perconditioning. Am J Physiol Heart Circ Physiol 2007;292:H1883-1890.
13. Kerendi F, Kin H, Halkos ME, Jiang R, Zatta AJ, Zhao ZQ, Guyton RA, 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.
14. Hausenloy DJ, Candilio L, Evans R, Ariti C, Jenkins DP, Kolvekar S, Knight R, Kunst G, Laing C, Nicholas J, Pepper J, Robertson S, Xenou M, Clayton T, Yellon DM, Investigators ET. Remote ischemic preconditioning and outcomes of cardiac surgery. N Engl J Med 2015;373:1408-1417.
15. Meybohm P, Bein B, Brosteanu O, Cremer J, Gruenewald M, Stoppe C, Coburn M, Schaelte G, Boning A, Niemann B, Roesner J, Kletzin F, Strouhal U, Reyher C, Laufenberg-Feldmann R, Ferner M, Brandes IF, Bauer M, Stehr SN, Kortgen A, Wittmann M, Baumgarten G, Meyer-Treschan T, Kienbaum P, Heringlake M, Schon J, Sander M, Treskatsch S, Smul T, Wolwender E, Schilling T, Fuernau G, Hasenclever D, Zacharowski K, Collaborators RIS. A multicenter trial of remote ischemic preconditioning for heart surgery. N Engl J Med 2015;373:1397-1407.
16. Garratt KN, Whittaker P, Przyklenk K. Remote ischemic conditioning and the long road to clinical translation: Lessons learned from ERICCA and RIPHeart. Circ Res 2016;118:1052-1054.
17. Wever KE, Hooijmans CR, Riksen NP, Sterenborg TB, Sena ES, Ritskes-Hoitinga M, Warle MC. Determinants of the efficacy of cardiac ischemic preconditioning: A systematic review and meta-analysis of animal studies. PLoS One 2015;10:e0142021.
18. van Hout GP, Jansen Of Lorkeers SJ, Wever KE, Sena ES, Kouwenberg LH, van Solinge WW, Macleod MR, Doevendans PA, Pasterkamp G, Chamuleau SA, Hoefer IE. Translational failure of anti-inflammatory compounds for myocardial infarction: A meta-analysis of large animal models. Cardiovasc Res 2016;109:240-248.
19. Lecour S, Botker HE, Condorelli G, Davidson SM, Garcia-Dorado D, Engel FB, Ferdinandy P, Heusch G, Madonna R, Ovize M, Ruiz-Meana M, Schulz R, Sluijter JP, Van Laake LW, Yellon DM, Hausenloy DJ. ESC working group cellular biology of the heart: Position paper: Improving the preclinical assessment of novel cardioprotective therapies. Cardiovasc Res 2014;104:399-411.
20. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: Explanation and elaboration. BMJ 2009;339:b2700.
21. O'Connor D, Green S, Higgins JPT. Chapter 5: Defining the review question and developing criteria for including studies. In JPT Higgins, S Green (eds). Cochrane Handbook for Systematic Reviews of Interventions Version 510. Haymarket, London: The Cochrane Collaboration; 2011.
22. Bell RM, Mocanu MM, Yellon DM. Retrograde heart perfusion: The Langendorff technique of isolated heart perfusion. J Mol Cell Cardiol 2011;50:940-950.
23. Rochitte CE, Azevedo CF. The myocardial area at risk. Heart 2012;98:348-350.
24. Ytrehus K, Liu Y, Tsuchida A, Miura T, Liu GS, Yang XM, Herbert D, Cohen MV, Downey JM. Rat and rabbit heart infarction: Effects of anesthesia, perfusate, risk zone, and method of infarct sizing. Am J Physiol 1994;267:H2383-2390.
25. Marber MS, Latchman DS, Walker JM, Yellon DM. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Circulation 1993;88:1264-1272.
26. Kuzuya T, Hoshida S, Yamashita N, Fuji H, Oe H, Hori M, Kamada T, Tada M. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia. Circ Res 1993;72:1293-1299.
27. Szekeres L, Papp JG, Szilvassy Z, Udvary E, Vegh A. Moderate stress by cardiac pacing may induce both short term and long term cardioprotection. Cardiovasc Res 1993;27:593-596.
28. Ovize M, Baxter GF, Di Lisa F, Ferdinandy P, Garcia-Dorado D, Hausenloy DJ, Heusch G, Vinten-Johansen J, Yellon DM, Schulz R. 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 2010;87:406-423.
29. Vesterinen HM, Sena ES, Egan KJ, Hirst TC, Churolov L, Currie GL, Antonic A, Howells DW, Macleod MR. Meta-analysis of data from animal studies: A practical guide. J Neurosci Methods 2014;221:92-102.
30. Loukogeorgakis SP, Williams R, Panagiotidou AT, Kolvekar SK, Donald A, Cole TJ, Yellon DM, Deanfield JE, MacAllister RJ. Transient limb ischemia induces remote preconditioning and remote postconditioning in humans by a K(ATP)-channel dependent mechanism. Circulation 2007;116:1386-1395.
31. Hooijmans CR, IntHout J, Ritskes-Hoitinga M, Rovers MM. Meta-analyses of animal studies: An introduction of a valuable instrument to further improve healthcare. ILAR J 2014;55:418-426.
32. Holm S. A simple sequentially rejective multiple test procedure. Scand J Stat 1979;6:65-70.
33. McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL. Guidelines for reporting experiments involving animals: The ARRIVE guidelines. Br J Pharmacol 2010;160:1573-1576.
34. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG. Animal research: Reporting in vivo experiments: The ARRIVE guidelines. Br J Pharmacol 2010;160:1577-1579.
35. Macleod MR, O'Collins T, Howells DW, Donnan GA. Pooling of animal experimental data reveals influence of study design and publication bias. Stroke 2004;35:1203-1208.
36. Samanta A, Dawn B. Remote ischemic preconditioning for cardiac surgery: Reflections on evidence of efficacy. Circ Res 2016;118:1055-1058.
37. Zaugg M, Lucchinetti E. Remote ischemic preconditioning in cardiac surgery-ineffective and risky N Engl J Med 2015;373:1470-1472.
38. Lim WY, Messow CM, Berry C. Cyclosporin variably and inconsistently reduces infarct size in experimental models of reperfused myocardial infarction: A systematic review and meta-analysis. Br J Pharmacol 2012;165:2034-2043.
39. Mewton N, Bergerot C, Ovize M. Cyclosporine before PCI in acute myocardial infarction. N Engl J Med 2016;374:90.
40. Lu Y, Dong CS, Yu JM, Li H. Morphine reduces the threshold of remote ischemic preconditioning against myocardial ischemia and reperfusion injury in rats: The role of opioid receptors. J Cardiothorac Vasc Anesth 2012;26:403-406.
41. Li CM, Zhang XH, Ma XJ, Luo M. Limb ischemic postconditioning protects myocardium from ischemia-reperfusion injury. Scand Cardiovasc J 2006;40:312-317.
42. Mastitskaya S, Marina N, Gourine A, Gilbey MP, Spyer KM, Teschemacher AG, Kasparov S, Trapp S, Ackland GL, Gourine AV. Cardioprotection evoked by remote ischaemic preconditioning is critically dependent on the activity of vagal preganglionic neurones. Cardiovasc Res 2012;95:487-494.
43. Weinbrenner C, Nelles M, Herzog N, Sarvary L, Strasser RH. Remote preconditioning by infrarenal occlusion of the aorta protects the heart from infarction: A newly identified non-neuronal but PKC-dependent pathway. Cardiovasc Res 2002;55:590-601.
44. Wever KE, Warle MC, Wagener FA, van der Hoorn JW, Masereeuw R, van der Vliet JA, Rongen GA. Remote ischaemic preconditioning by brief hind limb ischaemia protects against renal ischaemia-reperfusion injury: The role of adenosine. Nephrol Dial Transplant 2011;26:3108-3117.
45. Johnsen J, Pryds K, Salman R, Lofgren B, Kristiansen SB, Botker HE. The remote ischemic preconditioning algorithm: Effect of number of cycles, cycle duration and effector organ mass on efficacy of protection. Basic Res Cardiol 2016;111:10.
46. Wang F, Birch SE, He R, Tawadros P, Szaszi K, Kapus A, Rotstein OD. Remote ischemic preconditioning by hindlimb occlusion prevents liver ischemic/reperfusion injury: The role of high mobility group-box 1. Ann Surg 2010;251:292-299.
47. Rassaf T, Totzeck M, Hendgen-Cotta UB, Shiva S, Heusch G, Kelm M. Circulating nitrite contributes to cardioprotection by remote ischemic preconditioning. Circ Res 2014;114:1601-1610.
48. Lim SY, Yellon DM, Hausenloy DJ. The neural and humoral pathways in remote limb ischemic preconditioning. Basic Res Cardiol 2010;105:651-655.
49. Stub D, Smith K, Bernard S, Nehme Z, Stephenson M, Bray JE, Cameron P, Barger B, Ellims AH, Taylor AJ, Meredith IT, Kaye DM. Air versus oxygen in st-segmentelevation myocardial infarction. Circulation 2015;131:2143-2150.
50. Kleinbongard P, Neuhauser M, Thielmann M, Kottenberg E, Peters J, Jakob H, Heusch G. Confounders of cardioprotection by remote ischemic preconditioning in patients undergoing coronary artery bypass grafting. Cardiology 2016;133:128-133.
51. Kottenberg E, Thielmann M, Bergmann L, Heine T, Jakob H, Heusch G, Peters J. Protection by remote ischemic preconditioning during coronary artery bypass graft surgery with isoflurane but not propofol- A clinical trial. Acta Anaesthesiol Scand 2012;56:30-38.
52. Kottenberg E, Musiolik J, Thielmann M, Jakob H, Peters J, Heusch G. 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 2014;147:376-382.
53. Heusch G, Gersh BJ. ERICCA and RIPHeart: Two nails in the coffin for cardioprotection by remote ischemic conditioning Probably not! Eur Heart J 2016;37:200-202.
54. Alburquerque-Bejar JJ, Barba I, Inserte J, Miro-Casas E, Ruiz-Meana M, Poncelas M, Vilardosa U, Valls-Lacalle L, Rodriguez-Sinovas A, Garcia-Dorado D. Combination therapy with remote ischaemic conditioning and insulin or exenatide enhances infarct size limitation in pigs. Cardiovasc Res 2015;107:246-254.
55. Hausenloy DJ, Iliodromitis EK, Andreadou I, Papalois A, Gritsopoulos G, Anastasiou-Nana M, Kremastinos DT, Yellon DM. Investigating the signal transduction pathways underlying remote ischemic conditioning in the porcine heart. Cardiovasc Drugs Ther 2012;26:87-93.
56. Sachdeva J, Dai W, Gerczuk PZ, Kloner RA. Combined remote perconditioning and postconditioning failed to attenuate infarct size and contractile dysfunction in a rat model of coronary artery occlusion. J Cardiovasc Pharmacol Ther 2014;19: 567-573.
57. Hodgin JB, Maeda N. Minireview: Estrogen and mouse models of atherosclerosis. Endocrinology 2002;143:4495-4501.
58. Murphy E, Steenbergen C. Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury. Cardiovasc Res 2007;75:478-486.
59. Black SC, Rodger IW. Methods for studying experimental myocardial ischemic and reperfusion injury. J Pharmacol Toxicol Methods 1996;35:179-190.
60. Helisch A, Wagner S, Khan N, Drinane M, Wolfram S, Heil M, Ziegelhoeffer T, Brandt U, Pearlman JD, Swartz HM, Schaper W. Impact of mouse strain differences in innate hindlimb collateral vasculature. Arterioscler Thromb Vasc Biol 2006;26:520-526.
61. Black SC, Gralinski MR, Friedrichs GS, Kilgore KS, Driscoll EM, Lucchesi BR. Cardioprotective effects of heparin or N-acetylheparin in an in vivo model of myocardial ischaemic and reperfusion injury. Cardiovasc Res 1995;29:629-636.
62. Gralinski MR, Driscoll EM, Friedrichs GS, DeNardis MR, Lucchesi BR. Reduction of myocardial necrosis after glycosaminoglycan administration: Effects of a single intravenous administration of heparin or N-Acetylheparin 2 hours before regional ischemia and reperfusion. J Cardiovasc Pharmacol Ther 1996;1:219-228.
63. Barry WH, Kennedy TP. Heparins with reduced anti-coagulant activity reduce myocardial reperfusion injury. Recent Pat Cardiovasc Drug Discov 2011;6:148-157.
64. Kouretas PC, Kim YD, Cahill PA, Myers AK, To LN, Wang YN, Sitzmann JV, Hannan RL. Nonanticoagulant heparin prevents coronary endothelial dysfunction after brief ischemia-reperfusion injury in the dog. Circulation 1999;99:1062-1068.
65. Kouretas PC, Myers AK, Kim YD, Cahill PA, Myers JL, Wang YN, Sitzmann JV, Wallace RB, Hannan RL. Heparin and nonanticoagulant heparin preserve regional myocardial contractility after ischemia-reperfusion injury: Role of nitric oxide. J Thorac Cardiovasc Surg 1998;115:440-448; discussion 448-449.
66. Przyklenk K. Ischaemic conditioning: Pitfalls on the path to clinical translation. Br J Pharmacol 2015;172:1961-1973.
67. Hausenloy DJ, Erik Botker H, 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. 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 2013;98:7-27.
68. Jensen RV, Stottrup NB, Kristiansen SB, Botker HE. Release of a humoral circulating cardioprotective factor by remote ischemic preconditioning is dependent on preserved neural pathways in diabetic patients. Basic Res Cardiol 2012;107:285.
69. Baranyai T, Nagy CT, Koncsos G, Onodi Z, Karolyi-Szabo M, Makkos A, Varga ZV, Ferdinandy P, Giricz Z. Acute hyperglycemia abolishes cardioprotection by remote ischemic perconditioning. Cardiovasc Diabetol 2015;14:151.
70. Ferdinandy P, Hausenloy DJ, Heusch G, Baxter GF, Schulz R. Interaction of risk factors, comorbidities, and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning. Pharmacological reviews 2014;66:1142-1174.
71. van der Worp HB, Macleod MR. Preclinical studies of human disease: Time to take methodological quality seriously. J Mol Cell Cardiol 2011;51:449-450.
72. Sena ES, van der Worp HB, Bath PM, Howells DW, Macleod MR. Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS Biol 2010;8:e1000344.
73. van der Worp HB, Howells DW, Sena ES, Porritt MJ, Rewell S, O'Collins V, Macleod MR. Can animal models of disease reliably inform human studies PLoS Med 2010;7:e1000245.
74. Hirst JA, Howick J, Aronson JK, Roberts N, Perera R, Koshiaris C, Heneghan C. The need for randomization in animal trials: An overview of systematic reviews. PLoS One 2014;9:e98856.