Remote ischemic conditioning and cardioprotection: a systematic review and meta-analysis of randomized clinical trials

Basic Research in Cardiology

Volumn 110, Issue 2, 2015, Pages

  Le Page, Sophie ^a   Bejan Angoulvant, Theodora ^b   Angoulvant, Denis ^c   Prunier, Fabrice ^a  

^a ANGERS UNIVERSITY HOSPITAL   (France)

^b UNIVERSITÉ DE TOURS   (France)

^c UNIVERSITY HOSPITAL OF TOURS   (France)

Author keywords

Cardioprotection; Meta analysis; Myocardial injury; Randomized controlled trials; Remote ischemic conditioning; Systematic review

Indexed keywords

CREATINE KINASE MB; TROPONIN;

AREA UNDER THE CURVE; ARTICLE; CONDITIONING; CONGENITAL HEART DISEASE; CONTROLLED STUDY; CORONARY ARTERY BYPASS GRAFT; GENETIC HETEROGENEITY; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HORMONE RELEASE; HUMAN; INCIDENCE; META ANALYSIS; MORTALITY; NON ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; OUTCOME ASSESSMENT; PERCUTANEOUS CORONARY INTERVENTION; RANDOMIZED CONTROLLED TRIAL; REMOTE ISCHEMIC CONDITIONING; REPERFUSION INJURY; REVASCULARIZATION; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; TRANSLUMINAL CORONARY ANGIOPLASTY; HEART INFARCTION PREVENTION; ISCHEMIC POSTCONDITIONING; MYOCARDIAL REPERFUSION INJURY; PROCEDURES; RANDOMIZED CONTROLLED TRIAL (TOPIC);

HUMANS; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MYOCARDIAL REPERFUSION INJURY; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 84928254479     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-015-0467-8     Document Type: Article

References (86)

1. Ahmed RM, el Mohamed HA, Ashraf M, Maithili S, Nabil F, Rami R, Mohamed TI (2013) Effect of remote ischemic preconditioning on serum troponin T level following elective percutaneous coronary intervention. Catheter Cardiovasc Interv 82:E647–E653. doi:10.1002/ccd.24825
2. Albrecht M, Zitta K, Bein B, Wennemuth G, Broch O, Renner J, Schuett T, Lauer F, Maahs D, Hummitzsch L, Cremer J, Zacharowski K, Meybohm P (2013) Remote ischemic preconditioning regulates HIF-1alpha levels, apoptosis and inflammation in heart tissue of cardiosurgical patients: a pilot experimental study. Basic Res Cardiol 108:314. doi:10.1007/s00395-012-0314-0
3. Ali N, Rizwi F, Iqbal A, Rashid A (2010) Induced remote ischemic pre-conditioning on ischemia-reperfusion injury in patients undergoing coronary artery bypass. J Coll Physicians Surg Pak 20(7):427–431. doi:07.2010/jcpsp.427431
4. 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
5. Armijo-Olivo S, Ospina M, da Costa BR, Egger M, Saltaji H, Fuentes J, Ha C, Cummings GG (2014) Poor reliability between Cochrane reviewers and blinded external reviewers when applying the Cochrane risk of bias tool in physical therapy trials. PLoS One 9:e96920. doi:10.1371/journal.pone.0096920
6. Birnbaum Y, Hale SL, Kloner RA (1997) 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 96:1641–1646. doi:10.1161/01.CIR.96.5.1641
7. 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
8. Brener SJ, Lytle BW, Schneider JP, Ellis SG, Topol EJ (2002) Association between CK-MB elevation after percutaneous or surgical revascularization and three-year mortality. J Am Coll Cardiol 40:1961–1967. doi:10.1016/s0735-1097(02)02538-x
9. Brevoord D, Kranke P, Kuijpers M, Weber N, Hollmann M, Preckel B (2012) Remote ischemic conditioning to protect against ischemia-reperfusion injury: a systematic review and meta-analysis. PLoS One 7:e42179. doi:10.1371/journal.pone.0042179
10. Carrasco-Chinchilla F, Munoz-Garcia AJ, Dominguez-Franco A, Millan-Vazquez G, Guerrero-Molina A, Ortiz-Garcia C, Enguix-Armada A, Alonso-Briales JH, Hernandez-Garcia JM, de Teresa-Galvan E, Jimenez-Navarro MF (2013) Remote ischaemic postconditioning: does it protect against ischaemic damage in percutaneous coronary revascularisation? Randomised placebo-controlled clinical trial. Heart 99:1431–1437. doi:10.1136/heartjnl-2013-304172
11. Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, 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
12. Chia S, Senatore F, Raffel OC, Lee H, Wackers FJ, Jang IK (2008) Utility of cardiac biomarkers in predicting infarct size, left ventricular function, and clinical outcome after primary percutaneous coronary intervention for ST-segment elevation myocardial infarction. JACC Cardiovasc Interv 1:415–423. doi:10.1016/j.jcin.2008.04.010
13. Choi YS, Shim JK, Kim JC, Kang KS, Seo YH, Ahn KR, Kwak YL (2011) Effect of remote ischemic preconditioning on renal dysfunction after complex valvular heart surgery: a randomized controlled trial. J Thorac Cardiovasc Surg 142:148–154. doi:10.1016/j.jtcvs.2010.11.018
14. 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 Visconti L, 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
15. 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 Zoccai G, 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
16. 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
17. 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
18. Gerczuk PZ, Kloner RA (2012) An update on cardioprotection: a review of the latest adjunctive therapies to limit myocardial infarction size in clinical trials. J Am Coll Cardiol 59:969–978. doi:10.1016/j.jacc.2011.07.054
19. Ghaemian A, Nouraei SM, Abdollahian F, Naghshvar F, Giussani DA, Nouraei SA (2012) Remote ischemic preconditioning in percutaneous coronary revascularization: a double-blind randomized controlled clinical trial. Asian Cardiovasc Thorac Ann 20:548–554. doi:10.1177/0218492312439999
20. Gho BC, Schoemaker RG, van den Doel MA, Duncker DJ, Verdouw PD (1996) Myocardial protection by brief ischemia in noncardiac tissue. Circulation 94:2193–2200. doi:10.1161/01.CIR.94.9.2193
21. Gunaydin B, Cakici I, Soncul H, Kalaycioglu S, Cevik C, Sancak B, Kanzik I, Karadenizli Y (2000) Does remote organ ischaemia trigger cardiac preconditioning during coronary artery surgery? Pharmacol Res 41:493–496. doi:10.1006/phrs.1999.0611
22. Hartling L, Hamm MP, Milne A, Vandermeer B, Santaguida PL, Ansari M, Tsertsvadze A, Hempel S, Shekelle P, Dryden DM (2013) Testing the risk of bias tool showed low reliability between individual reviewers and across consensus assessments of reviewer pairs. J Clin Epidemiol 66:973–981. doi:10.1016/j.jclinepi.2012.07.005
23. 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 (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
24. 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
25. Healy DA, Khan WA, Wong CS, Moloney MC, Grace PA, Coffey JC, Dunne C, Walsh SR, Sadat U, Gaunt ME, Chen S, Tehrani S, Hausenloy DJ, Yellon DM, Kramer RS, Zimmerman RF, Lomivorotov VV, Shmyrev VA, Ponomarev DN, Rahman IA, Mascaro JG, Bonser RS, Jeon Y, Hong DM, Wagner R, Thielmann M, Heusch G, Zacharowski K, Meybohm P, Bein B, Tang TY (2014) Remote preconditioning and major clinical complications following adult cardiovascular surgery: systematic review and meta-analysis. Int J Cardiol 176:20–31. doi:10.1016/j.ijcard.2014.06.018
26. Heusch G (2013) Cardioprotection: chances and challenges of its translation to the clinic. Lancet 381:166–175. doi:10.1016/s0140-6736(12)60916-7
27. Heusch G, Bøtker HE, Przyklenk K, Redington A, Yellon D (2015) Remote Ischemic Conditioning. J Am Coll Cardiol 65:177–195. doi:10.1016/j.jacc.2014.10.031
28. Heusch G, Musiolik J, Kottenberg E, Peters J, Jakob H, Thielmann M (2012) STAT5 activation and cardioprotection by remote ischemic preconditioning in humans: short communication. Circ Res 110:111–115. doi:10.1161/circresaha.111.259556
29. Higgins JPT, Green S (eds) (2011) Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org
30. Higgins JP, White IR, Anzures-Cabrera J (2008) Meta-analysis of skewed data: combining results reported on log-transformed or raw scales. Stat Med 27:6072–6092. doi:10.1002/sim.3427
31. Hong DM, Jeon Y, Lee CS, Kim HJ, Lee JM, Bahk JH, Kim KB, Hwang HY (2012) Effects of remote ischemic preconditioning with postconditioning in patients undergoing off-pump coronary artery bypass surgery–randomized controlled trial. Circ J 76:884–890. doi:10.1253/circj.CJ-11-1068
32. Hong DM, Lee EH, Kim HJ, Min JJ, Chin JH, Choi DK, Bahk JH, Sim JY, Choi IC, Jeon Y (2013) 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
33. Hong DM, Mint JJ, Kim JH, Sohn IS, Lim TW, Lim YJ, Bahk JH, Jeon Y (2010) The effect of remote ischaemic preconditioning on myocardial injury in patients undergoing off-pump coronary artery bypass graft surgery. Anaesth Intensive Care 38:924–929
34. Hoole SP, 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
35. Hoole SP, Khan SN, White PA, Heck PM, Kharbanda RK, Densem CG, Clarke SC, Shapiro LM, Schofield PM, O’Sullivan M, Dutka DP (2009) Remote ischaemic pre-conditioning does not attenuate ischaemic left ventricular dysfunction in humans. Eur J Heart Fail 11:497–505. doi:10.1093/eurjhf/hfp040
36. Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5:13. doi:10.1186/1471-2288-5-13
37. 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
38. Jones BO, Pepe S, Sheeran FL, Donath S, Hardy P, Shekerdemian L, Penny DJ, McKenzie I, Horton S, Brizard CP, d’Udekem Y, Konstantinov IE, Cheung MM (2013) Remote ischemic preconditioning in cyanosed neonates undergoing cardiopulmonary bypass: a randomized controlled trial. J Thorac Cardiovasc Surg 146:1334–1340. doi:10.1016/j.jtcvs.2013.01.003
39. 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
40. Kathiresan S, Servoss SJ, Newell JB, Trani D, MacGillivray TE, Lewandrowski K, Lee-Lewandrowski E, Januzzi JL Jr (2004) Cardiac troponin T elevation after coronary artery bypass grafting is associated with increased one-year mortality. Am J Cardiol 94:879–881. doi:10.1016/j.amjcard.2004.06.022
41. Kharbanda RK, Mortensen UM, White PA, Kristiansen SB, Schmidt MR, Hoschtitzky JA, Vogel M, Sorensen K, Redington AN, MacAllister R (2002) Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation 106:2881–2883. doi:10.1161/01.CIR.0000043806.51912.9B
42. 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
43. 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
44. 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
45. 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
46. Lee JH, Park YH, Byon HJ, Kim HS, Kim CS, Kim JT (2012) Effect of remote ischaemic preconditioning on ischaemic-reperfusion injury in pulmonary hypertensive infants receiving ventricular septal defect repair. Br J Anaesth 108:223–228. doi:10.1093/bja/aer388
47. Li L, Luo W, Huang L, Zhang W, Gao Y, Jiang H, Zhang C, Long L, Chen S (2010) Remote perconditioning reduces myocardial injury in adult valve replacement: a randomized controlled trial. J Surg Res 164:e21–e26. doi:10.1016/j.jss.2010.06.016
48. Lim SY, Hausenloy DJ (2012) Remote ischemic conditioning: from bench to bedside. Front Physiol 3:27. doi:10.3389/fphys.2012.00027
49. Lim SY, Yellon DM, Hausenloy DJ (2010) The neural and humoral pathways in remote limb ischemic preconditioning. Basic Res Cardiol 105:651–655. doi:10.1007/s00395-010-0099-y
50. Lomivorotov VV, Shmyrev VA, Nepomnyaschih VA, Ponomarev DN, Knyazkova LG, Lomivorotov VN, Karaskov AM (2012) Remote ischaemic preconditioning does not protect the heart in patients undergoing coronary artery bypass grafting. Interact CardioVasc Thorac Surg 15:18–22. doi:10.1093/icvts/ivs118
51. Lucchinetti E, Bestmann L, Feng J, Freidank H, Clanachan AS, Finegan BA, Zaugg M (2012) Remote ischemic preconditioning applied during isoflurane inhalation provides no benefit to the myocardium of patients undergoing on-pump coronary artery bypass graft surgery: lack of synergy or evidence of antagonism in cardioprotection? Anesthesiology 116:296–310. doi:10.1097/ALN.0b013e318242349a
52. Luo SJ, Zhou YJ, Shi DM, Ge HL, Wang JL, Liu RF (2013) Remote ischemic preconditioning reduces myocardial injury in patients undergoing coronary stent implantation. Can J Cardiol 29:1084–1089. doi:10.1016/j.cjca.2012.11.022
53. Luo W, Zhu M, Huang R, Zhang Y (2011) A comparison of cardiac post-conditioning and remote pre-conditioning in paediatric cardiac surgery. Cardiol Young 21:266–270. doi:10.1017/s1047951110001915
54. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6:e1000097. doi:10.1371/journal.pmed.1000097
55. Munk K, Andersen NH, Schmidt MR, Nielsen SS, Terkelsen CJ, Sloth E, Botker HE, Nielsen TT, Poulsen SH (2010) Remote ischemic conditioning in patients With myocardial infarction treated with primary angioplasty: impact on left ventricular function assessed by comprehensive echocardiography and gated single-photon emission CT. Circ Cardiovasc Imaging 3:656–662. doi:10.1161/circimaging.110.957340
56. Muntean DM, Ordodi V, Ferrera R, Angoulvant D (2013) Volatile anaesthetics and cardioprotection: lessons from animal studies. Fundam Clin Pharmacol 27:21–34. doi:10.1111/j.1472-8206.2012.01055.x
57. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136. doi:10.1161/01.CIR.74.5.1124
58. Pavione MA, Carmona F, de Castro M, Carlotti AP (2012) Late remote ischemic preconditioning in children undergoing cardiopulmonary bypass: a randomized controlled trial. J Thorac Cardiovasc Surg 144:178–183. doi:10.1016/j.jtcvs.2011.12.029
59. Pell TJ, Baxter GF, Yellon DM, Drew GM (1998) Renal ischemia preconditions myocardium: role of adenosine receptors and ATP-sensitive potassium channels. Am J Physiol 275:H1542–H1547
60. Pepe S, Liaw NY, Hepponstall M, Sheeran FL, Yong MS, d’Udekem Y, Cheung MM, Konstantinov IE (2013) Effect of remote ischemic preconditioning on phosphorylated protein signaling in children undergoing tetralogy of fallot repair: a randomized controlled trial. J Am Heart Assoc 2:e000095. doi:10.1161/jaha.113.000095
61. Pickard JM, Botker HE, Crimi G, Davidson B, Davidson SM, Dutka D, Ferdinandy P, Ganske R, Garcia-Dorado D, Giricz Z, Gourine AV, Heusch G, Kharbanda R, Kleinbongard P, MacAllister R, McIntyre C, Meybohm P, Prunier F, Redington A, Robertson NJ, Suleiman MS, Vanezis A, Walsh S, Yellon DM, Hausenloy DJ (2015) Remote ischemic conditioning: from experimental observation to clinical application: report from the 8th Biennial Hatter Cardiovascular Institute Workshop. Basic Res Cardiol 110:453. doi:10.1007/s00395-014-0453-6
62. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N, Elbelghiti R, Cung TT, Bonnefoy E, Angoulvant D, Macia C, Raczka F, Sportouch C, Gahide G, Finet G, Andre-Fouet X, Revel D, Kirkorian G, Monassier JP, Derumeaux G, Ovize M (2008) Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 359:473–481. doi:10.1056/NEJMoa071142
63. Prasad A, Gossl M, Hoyt J, Lennon RJ, Polk L, Simari R, Holmes DR Jr, Rihal CS, Lerman A (2013) Remote ischemic preconditioning immediately before percutaneous coronary intervention does not impact myocardial necrosis, inflammatory response, and circulating endothelial progenitor cell counts: a single center randomized sham controlled trial. Catheter Cardiovasc Interv 81:930–936. doi:10.1002/ccd.24443
64. Prunier F, Angoulvant D, Saint Etienne C, 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
65. Przyklenk K, Bauer B, Ovize M, Kloner RA, Whittaker P (1993) Regional ischemic ‘preconditioning’ protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation 87:893–899. doi:10.1161/01.CIR.87.3.893
66. 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.109.926667
67. 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
68. Saxena P, Aggarwal S, Misso NL, Passage J, Newman MA, Thompson PJ, d’Udekem Y, Praporski S, Konstantinov IE (2013) Remote ischaemic preconditioning down-regulates kinin receptor expression in neutrophils of patients undergoing heart surgery. Interact CardioVasc Thorac Surg 17:653–658. doi:10.1093/icvts/ivt279
69. Schevchuck A, Laskey WK (2013) Ischemic conditioning as an adjunct to percutaneous coronary intervention. Circ Cardiovasc Interv 6:484–492. doi:10.1161/circinterventions.113.000146
70. Slagsvold KH, Rognmo O, Hoydal M, Wisloff U, Wahba A (2014) Remote ischemic preconditioning preserves mitochondrial function and influences myocardial MicroRNA expression in atrial myocardium during coronary bypass surgery. Circ Res 114:851–859. doi:10.1161/circresaha.114.302751
71. Sloth AD, Schmidt MR, Munk K, Kharbanda RK, Redington AN, Schmidt M, Pedersen L, Sorensen HT, Botker HE (2013) 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
72. 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
73. 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
74. Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR, White HD, Thygesen K, Alpert JS, White HD, Jaffe AS, Katus HA, Apple FS, Lindahl B, Morrow DA, Chaitman BA, Clemmensen PM, Johanson P, Hod H, Underwood R, Bax JJ, Bonow RO, Pinto F, Gibbons RJ, Fox KA, Atar D, Newby LK, Galvani M, Hamm CW, Uretsky BF, Steg PG, Wijns W, Bassand JP, Menasche P, Ravkilde J, Ohman EM, Antman EM, Wallentin LC, Armstrong PW, Simoons ML, Januzzi JL, Nieminen MS, Gheorghiade M, Filippatos G, Luepker RV, Fortmann SP, Rosamond WD, Levy D, Wood D, Smith SC, Hu D, Lopez-Sendon JL, Robertson RM, Weaver D, Tendera M, Bove AA, Parkhomenko AN, Vasilieva EJ, Mendis S (2012) Third universal definition of myocardial infarction. Eur Heart J 33:2551–2567. doi:10.1093/eurheartj/ehs184
75. Tzivoni D, Koukoui D, Guetta V, Novack L, Cowing G (2008) Comparison of Troponin T to creatine kinase and to radionuclide cardiac imaging infarct size in patients with ST-elevation myocardial infarction undergoing primary angioplasty. Am J Cardiol 101:753–757. doi:10.1016/j.amjcard.2007.09.119
76. Venugopal V, Hausenloy DJ, Ludman A, Di Salvo C, Kolvekar S, Yap J, Lawrence D, Bognolo J, Yellon DM (2009) Remote ischaemic preconditioning reduces myocardial injury in patients undergoing cardiac surgery with cold-blood cardioplegia: a randomised controlled trial. Heart 95:1567–1571. doi:10.1136/hrt.2008.155770
77. Wagner R, Piler P, Bedanova H, Adamek P, Grodecka L, Freiberger T (2010) Myocardial injury is decreased by late remote ischaemic preconditioning and aggravated by tramadol in patients undergoing cardiac surgery: a randomised controlled trial. Interact CardioVasc Thorac Surg 11:758–762. doi:10.1510/icvts.2010.243600
78. 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
79. Walsh SR, Nouraei SA, Tang TY, Sadat U, Carpenter RH, Gaunt ME (2010) Remote ischemic preconditioning for cerebral and cardiac protection during carotid endarterectomy: results from a pilot randomized clinical trial. Vasc Endovascular Surg 44:434–439. doi:10.1177/1538574410369709
80. Wu Q, Gui P, Wu J, Ding D, Purusram G, Dong N, Yao S (2011) Effect of limb ischemic preconditioning on myocardial injury in patients undergoing mitral valve replacement surgery. A randomized controlled trial. Circ J 75:1885–1889. doi:10.1253/circj.CJ-10-1130
81. Xie JJ, Liao XL, Chen WG, Huang DD, Chang FJ, Chen W, Luo ZL, Wang ZP, Ou JS (2012) Remote ischaemic preconditioning reduces myocardial injury in patients undergoing heart valve surgery: randomised controlled trial. Heart 98:384–388. doi:10.1136/heartjnl-2011-300860
82. Yetgin T, Manintveld OC, Boersma E, Kappetein AP, van Geuns RJ, Zijlstra F, Duncker DJ, van der Giessen WJ (2012) Remote ischemic conditioning in percutaneous coronary intervention and coronary artery bypass grafting. Circ J 76:2392–2404. doi:10.1253/circj.CJ-12-0518
83. Young PJ, Dalley P, Garden A, Horrocks C, La Flamme A, Mahon B, Miller J, Pilcher J, Weatherall M, Williams J, Young W, Beasley R (2012) 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 107:256. doi:10.1007/s00395-012-0256-6
84. Zeng J, He W, Qu Z, Tang Y, Zhou Q, Zhang B (2014) Cold blood versus crystalloid cardioplegia for myocardial protection in adult cardiac surgery: a meta-analysis of randomized controlled studies. J Cardiothorac Vasc Anesth 28:674–681. doi:10.1053/j.jvca.2013.06.005
85. Zhong H, Gao Z, Chen M, Zhao J, Wang F, Li L, Dong H, Liu L, Wang Q, Xiong L (2013) Cardioprotective effect of remote ischemic postconditioning on children undergoing cardiac surgery: a randomized controlled trial. Paediatr Anaesth 23:726–733. doi:10.1111/pan.12181
86. Zhou W, Zeng D, Chen R, Liu J, Yang G, Liu P, Zhou X (2010) Limb ischemic preconditioning reduces heart and lung injury after an open heart operation in infants. Pediatr Cardiol 31:22–29. doi:10.1007/s00246-009-9536-9