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Semin Thromb Hemost 2017; 43(07): 716-731
DOI: 10.1055/s-0037-1604088
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Ischemic Conditioning as a Hemostatic Intervention in Surgery and Cardiac Procedures: A Systematic Review

Andreas Engel Krag
1   Department of Clinical Biochemistry, Center for Hemophilia and Thrombosis, Aarhus University Hospital, Aarhus N, Denmark
,
Anne-Mette Hvas
1   Department of Clinical Biochemistry, Center for Hemophilia and Thrombosis, Aarhus University Hospital, Aarhus N, Denmark
› Author Affiliations
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Publication History

Publication Date:
06 September 2017 (online)

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Abstract

Ischemic conditioning induced by nonlethal cycles of tissue ischemia and reperfusion attenuates ischemia–reperfusion injury. The objective of this study is to systematically review the effects of local and remote ischemic conditioning on laboratory parameters of hemostasis and the clinical outcomes of thromboembolism or bleeding in patients undergoing surgery or cardiac procedures. PubMed and Embase were searched for relevant human trials published in English between January 1, 1986, and September 7, 2016, and additional studies were identified from reference lists. Data on laboratory parameters of hemostasis, thromboembolism, and bleeding were extracted for qualitative synthesis. In total, 69 studies were included; of these, 53 were randomized controlled trials (RCTs) and 11 were meta-analyses. Local and remote ischemic conditioning reduced platelet activation in patients undergoing cardiac procedures. Local ischemic conditioning did not reduce the thromboembolic risk in patients undergoing surgery or cardiac procedures. Remote ischemic conditioning reduced the incidence of arterial thromboembolism after surgery or cardiac procedures in 3 out of 28 RCTs and 4 out of 5 meta-analyses. Local and remote ischemic conditioning did not increase operative bleeding. In conclusion, ischemic conditioning reduced platelet activity without increasing the risk of bleeding in patients undergoing surgery or cardiac procedures. Limited evidence supports the proposal that ischemic conditioning reduces the incidence of arterial thromboembolism in patients undergoing surgery or cardiac procedures.

Keywords

ischemic conditioning - hemostasis - thromboembolism - bleeding - surgery
 

  • References

  • 1 Cerra FB, Lajos TZ, Montes M, Siegel JH. Hemorrhagic infarction: a reperfusion injury following prolonged myocardial ischemic anoxia. Surgery 1975; 78 (01) 95-104
    PubMedGoogle Scholar
  • 2 Ritschel VN, Seljeflot I, Arnesen H. , et al. IL-6 signalling in patients with acute ST-elevation myocardial infarction. Results Immunol 2013; 4: 8-13
    PubMedGoogle Scholar
  • 3 Hansen CH, Ritschel V, Halvorsen S. , et al. Markers of thrombin generation are associated with myocardial necrosis and left ventricular impairment in patients with ST-elevation myocardial infarction. Thromb J 2015; 13: 31
    PubMedGoogle Scholar
  • 4 Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986; 74 (05) 1124-1136
    CrossrefPubMedGoogle Scholar
  • 5 Zhao ZQ, Corvera JS, Halkos ME. , et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 2003; 285 (02) H579-H588
    CrossrefPubMedGoogle Scholar
  • 6 Kharbanda RK, Mortensen UM, White PA. , et al. Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation 2002; 106 (23) 2881-2883
    CrossrefPubMedGoogle Scholar
  • 7 Bøtker HE, Kharbanda R, Schmidt MR. , 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 (9716): 727-734
    CrossrefPubMedGoogle Scholar
  • 8 Schmidt MR, Smerup M, Konstantinov IE. , et al. 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 (04) H1883-H1890
    CrossrefPubMedGoogle Scholar
  • 9 Kerendi F, Kin H, Halkos ME. , et al. 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 (05) 404-412
    CrossrefPubMedGoogle Scholar
  • 10 Clavien PA, Yadav S, Sindram D, Bentley RC. Protective effects of ischemic preconditioning for liver resection performed under inflow occlusion in humans. Ann Surg 2000; 232 (02) 155-162
    CrossrefPubMedGoogle Scholar
  • 11 Thielmann M, Kottenberg E, Boengler K. , et al. Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass surgery with crystalloid cardioplegic arrest. Basic Res Cardiol 2010; 105 (05) 657-664
    CrossrefPubMedGoogle Scholar
  • 12 Hausenloy DJ, Candilio L, Evans R. , et al; ERICCA Trial Investigators. Remote ischemic preconditioning and outcomes of cardiac surgery. N Engl J Med 2015; 373 (15) 1408-1417
    CrossrefPubMedGoogle Scholar
  • 13 Meybohm P, Bein B, Brosteanu O. , et al; RIPHeart Study Collaborators. A multicenter trial of remote ischemic preconditioning for heart surgery. N Engl J Med 2015; 373 (15) 1397-1407
    CrossrefPubMedGoogle Scholar
  • 14 Sloth AD, Schmidt MR, Munk K. , et al; 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 (03) 168-175
    CrossrefPubMedGoogle Scholar
  • 15 Dickson EW, Reinhardt CP, Renzi FP, Becker RC, Porcaro WA, Heard SO. Ischemic preconditioning may be transferable via whole blood transfusion: preliminary evidence. J Thromb Thrombolysis 1999; 8 (02) 123-129
    CrossrefPubMedGoogle Scholar
  • 16 Addison PD, Neligan PC, Ashrafpour H. , et al. Noninvasive remote ischemic preconditioning for global protection of skeletal muscle against infarction. Am J Physiol Heart Circ Physiol 2003; 285 (04) H1435-H1443
    CrossrefPubMedGoogle Scholar
  • 17 Lim SY, Yellon DM, Hausenloy DJ. The neural and humoral pathways in remote limb ischemic preconditioning. Basic Res Cardiol 2010; 105 (05) 651-655
    CrossrefPubMedGoogle Scholar
  • 18 Røpcke DM, Hjortdal VE, Toft GE, Jensen MO, Kristensen SD. Remote ischemic preconditioning reduces thrombus formation in the rat. J Thromb Haemost 2012; 10 (11) 2405-2406
    CrossrefPubMedGoogle Scholar
  • 19 Pedersen CM, Cruden NL, Schmidt MR. , et al. Remote ischemic preconditioning prevents systemic platelet activation associated with ischemia-reperfusion injury in humans. J Thromb Haemost 2011; 9 (02) 404-407
    CrossrefPubMedGoogle Scholar
  • 20 Battipaglia I, Scalone G, Milo M, Di Franco A, Lanza GA, Crea F. Upper arm intermittent ischaemia reduces exercise-related increase of platelet reactivity in patients with obstructive coronary artery disease. Heart 2011; 97 (16) 1298-1303
    CrossrefPubMedGoogle Scholar
  • 21 Hepponstall M, Ignjatovic V, Binos S. , et al. Remote ischemic preconditioning (RIPC) modifies plasma proteome in humans. PLoS One 2012; 7 (11) e48284
    CrossrefPubMedGoogle Scholar
  • 22 Pang T, Zhao Y, Zhang NR, Jin SQ, Pan SQ. Transient limb ischemia alters serum protein expression in healthy volunteers: complement C3 and vitronectin may be involved in organ protection induced by remote ischemic preconditioning. Oxid Med Cell Longev 2013; 2013: 859056
    PubMedGoogle Scholar
  • 23 Kristiansen J, Grove EL, Rise N. , et al. Effect of remote ischaemic conditioning on coagulation and fibrinolysis. Thromb Res 2016; 141: 129-135
    CrossrefPubMedGoogle Scholar
  • 24 Pedersen CM, Barnes G, Schmidt MR. , et al. Ischaemia-reperfusion injury impairs tissue plasminogen activator release in man. Eur Heart J 2012; 33 (15) 1920-1927
    CrossrefPubMedGoogle Scholar
  • 25 Pryds K, Kristiansen J, Neergaard-Petersen S. , et al. Effect of long-term remote ischaemic conditioning on platelet function and fibrinolysis in patients with chronic ischaemic heart failure. Thromb Res 2017; 153: 40-46
    CrossrefPubMedGoogle Scholar
  • 26 Meng R, Ding Y, Asmaro K. , et al. Ischemic conditioning is safe and effective for octo- and nonagenarians in stroke prevention and treatment. Neurotherapeutics 2015; 12 (03) 667-677
    CrossrefPubMedGoogle Scholar
  • 27 Meng R, Asmaro K, Meng L. , et al. Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 2012; 79 (18) 1853-1861
    CrossrefPubMedGoogle Scholar
  • 28 Gibbs NM, Crawford GP, Michalopoulos N. Postoperative changes in coagulant and anticoagulant factors following abdominal aortic surgery. J Cardiothorac Vasc Anesth 1992; 6 (06) 680-685
    CrossrefPubMedGoogle Scholar
  • 29 Moher D, Liberati A, Tetzlaff J, Altman DG. ; PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement. PLoS Med 2009; 6 (07) e1000097
    CrossrefPubMedGoogle Scholar
  • 30 Ye B, Zhao H, Hou H. , et al. Ischemic preconditioning provides no additive clinical value in liver resection of cirrhotic and non-cirrhotic patients under portal triad clamping: a prospective randomized controlled trial. Clin Res Hepatol Gastroenterol 2014; 38 (04) 467-474
    CrossrefPubMedGoogle Scholar
  • 31 Jeon J, Watkins A, Wagener G. , et al. Complex hepatectomy under total vascular exclusion of the liver: impact of ischemic preconditioning on clinical outcomes. World J Surg 2013; 37 (04) 838-846
    CrossrefPubMedGoogle Scholar
  • 32 Winbladh A, Björnsson B, Trulsson L, Offenbartl K, Gullstrand P, Sandström P. Ischemic preconditioning prior to intermittent Pringle maneuver in liver resections. J Hepatobiliary Pancreat Sci 2012; 19 (02) 159-170
    CrossrefPubMedGoogle Scholar
  • 33 Scatton O, Zalinski S, Jegou D. , et al. Randomized clinical trial of ischaemic preconditioning in major liver resection with intermittent Pringle manoeuvre. Br J Surg 2011; 98 (09) 1236-1243
    CrossrefPubMedGoogle Scholar
  • 34 Arkadopoulos N, Kostopanagiotou G, Theodoraki K. , et al. Ischemic preconditioning confers antiapoptotic protection during major hepatectomies performed under combined inflow and outflow exclusion of the liver. A randomized clinical trial. World J Surg 2009; 33 (09) 1909-1915
    CrossrefPubMedGoogle Scholar
  • 35 Heizmann O, Loehe F, Volk A, Schauer RJ. Ischemic preconditioning improves postoperative outcome after liver resections: a randomized controlled study. Eur J Med Res 2008; 13 (02) 79-86
    Google Scholar
  • 36 Azoulay D, Lucidi V, Andreani P. , et al. Ischemic preconditioning for major liver resection under vascular exclusion of the liver preserving the caval flow: a randomized prospective study. J Am Coll Surg 2006; 202 (02) 203-211
    CrossrefPubMedGoogle Scholar
  • 37 Choukèr A, Schachtner T, Schauer R. , et al. Effects of Pringle manoeuvre and ischaemic preconditioning on haemodynamic stability in patients undergoing elective hepatectomy: a randomized trial. Br J Anaesth 2004; 93 (02) 204-211
    CrossrefPubMedGoogle Scholar
  • 38 Memtsoudis SG, Valle AG, Jules-Elysse K. , et al. Perioperative inflammatory response in total knee arthroplasty patients: impact of limb preconditioning. Reg Anesth Pain Med 2010; 35 (05) 412-416
    CrossrefPubMedGoogle Scholar
  • 39 Memtsoudis SG, Stundner O, Yoo D. , et al. Does limb preconditioning reduce pain after total knee arthroplasty? A randomized, double-blind study. Clin Orthop Relat Res 2014; 472 (05) 1467-1474
    CrossrefPubMedGoogle Scholar
  • 40 Hahn JY, Song YB, Kim EK. , et al. Ischemic postconditioning during primary percutaneous coronary intervention: the effects of postconditioning on myocardial reperfusion in patients with ST-segment elevation myocardial infarction (POST) randomized trial. Circulation 2013; 128 (17) 1889-1896
    CrossrefPubMedGoogle Scholar
  • 41 Lee TM, Lin MS, Tsai CH, Chang NC. Effect of ischaemic preconditioning on regional release of inflammatory markers. Clin Sci (Lond) 2005; 109 (03) 267-276
    CrossrefPubMedGoogle Scholar
  • 42 Ji Q, Mei Y, Wang X. , et al. Effect of ischemic postconditioning in correction of tetralogy of Fallot. Int Heart J 2011; 52 (05) 312-317
    CrossrefPubMedGoogle Scholar
  • 43 Ji B, Liu M, Liu J. , et al. Evaluation by cardiac troponin I: the effect of ischemic preconditioning as an adjunct to intermittent blood cardioplegia on coronary artery bypass grafting. J Card Surg 2007; 22 (05) 394-400
    CrossrefPubMedGoogle Scholar
  • 44 Li G, Chen S, Lu E, Luo W. Cardiac ischemic preconditioning improves lung preservation in valve replacement operations. Ann Thorac Surg 2001; 71 (02) 631-635
    CrossrefPubMedGoogle Scholar
  • 45 Thomas KN, Cotter JD, Williams MJ, van Rij AM. Repeated episodes of remote ischemic preconditioning for the prevention of myocardial injury in vascular surgery. Vasc Endovascular Surg 2016; 50 (03) 140-146
    CrossrefPubMedGoogle Scholar
  • 46 Healy DA, Boyle E, McCartan D. , et al; Preconditioning Shields Against Vascular Events in Surgery (Preconditioning SAVES) Trial Group. A multicenter pilot randomized controlled trial of remote ischemic preconditioning in major vascular surgery. Vasc Endovascular Surg 2015; 49 (08) 220-227
    CrossrefPubMedGoogle Scholar
  • 47 Murphy N, Vijayan A, Frohlich S. , et al. Remote ischemic preconditioning does not affect the incidence of acute kidney injury after elective abdominal aortic aneurysm repair. J Cardiothorac Vasc Anesth 2014; 28 (05) 1285-1292
    CrossrefPubMedGoogle Scholar
  • 48 Li C, Li YS, Xu M. , et al. Limb remote ischemic preconditioning for intestinal and pulmonary protection during elective open infrarenal abdominal aortic aneurysm repair: a randomized controlled trial. Anesthesiology 2013; 118 (04) 842-852
    CrossrefPubMedGoogle Scholar
  • 49 Walsh SR, Sadat U, Boyle JR. , et al. Remote ischemic preconditioning for renal protection during elective open infrarenal abdominal aortic aneurysm repair: randomized controlled trial. Vasc Endovascular Surg 2010; 44 (05) 334-340
    CrossrefPubMedGoogle Scholar
  • 50 Walsh SR, Nouraei SA, Tang TY, Sadat U, Carpenter RH, Gaunt ME. Remote ischemic preconditioning for cerebral and cardiac protection during carotid endarterectomy: results from a pilot randomized clinical trial. Vasc Endovascular Surg 2010; 44 (06) 434-439
    CrossrefPubMedGoogle Scholar
  • 51 Walsh SR, Boyle JR, Tang TY. , et al. Remote ischemic preconditioning for renal and cardiac protection during endovascular aneurysm repair: a randomized controlled trial. J Endovasc Ther 2009; 16 (06) 680-689
    CrossrefPubMedGoogle Scholar
  • 52 Ali ZA, Callaghan CJ, Lim E. , et al. Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial. Circulation 2007; 116 (11, Suppl): I98-I105
    CrossrefPubMedGoogle Scholar
  • 53 Nicholson ML, Pattenden CJ, Barlow AD, Hunter JP, Lee G, Hosgood SA. A double blind randomized clinical trial of remote ischemic conditioning in live donor renal transplantation. Medicine (Baltimore) 2015; 94 (31) e1316
    CrossrefPubMedGoogle Scholar
  • 54 Kim WH, Lee JH, Ko JS. , et al. Effect of remote ischemic postconditioning on patients undergoing living donor liver transplantation. Liver Transpl 2014; 20 (11) 1383-1392
    CrossrefPubMedGoogle Scholar
  • 55 Li C, Xu M, Wu Y, Li YS, Huang WQ, Liu KX. Limb remote ischemic preconditioning attenuates lung injury after pulmonary resection under propofol-remifentanil anesthesia: a randomized controlled study. Anesthesiology 2014; 121 (02) 249-259
    CrossrefPubMedGoogle Scholar
  • 56 Walsh M, Whitlock R, Garg AX. , et al; Remote IMPACT Investigators. Effects of remote ischemic preconditioning in high-risk patients undergoing cardiac surgery (Remote IMPACT): a randomized controlled trial. CMAJ 2016; 188 (05) 329-336
    CrossrefPubMedGoogle Scholar
  • 57 Candilio L, Malik A, Ariti C. , et al. Effect of remote ischaemic preconditioning on clinical outcomes in patients undergoing cardiac bypass surgery: a randomised controlled clinical trial. Heart 2015; 101 (03) 185-192
    CrossrefPubMedGoogle Scholar
  • 58 Krogstad LE, Slagsvold KH, Wahba A. Remote ischemic preconditioning and incidence of postoperative atrial fibrillation. Scand Cardiovasc J 2015; 49 (03) 117-122
    CrossrefPubMedGoogle Scholar
  • 59 Hong DM, Lee EH, Kim HJ. , et al. 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 (03) 176-183
    CrossrefPubMedGoogle Scholar
  • 60 Hong DM, Jeon Y, Lee CS. , et al. Effects of remote ischemic preconditioning with postconditioning in patients undergoing off-pump coronary artery bypass surgery--randomized controlled trial. Circ J 2012; 76 (04) 884-890
    CrossrefPubMedGoogle Scholar
  • 61 Lucchinetti E, Bestmann L, Feng J. , et al. 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 2012; 116 (02) 296-310
    CrossrefPubMedGoogle Scholar
  • 62 Lavi S, D'Alfonso S, Diamantouros P. , et al. Remote ischemic postconditioning during percutaneous coronary interventions: remote ischemic postconditioning-percutaneous coronary intervention randomized trial. Circ Cardiovasc Interv 2014; 7 (02) 225-232
    CrossrefPubMedGoogle Scholar
  • 63 Xu X, Zhou Y, Luo S. , et al. Effect of remote ischemic preconditioning in the elderly patients with coronary artery disease with diabetes mellitus undergoing elective drug-eluting stent implantation. Angiology 2014; 65 (08) 660-666
    CrossrefPubMedGoogle Scholar
  • 64 Ahmed RM, Mohamed HA, Ashraf M. , et al. Effect of remote ischemic preconditioning on serum troponin T level following elective percutaneous coronary intervention. Catheter Cardiovasc Interv 2013; 82 (05) E647-E653
    CrossrefPubMedGoogle Scholar
  • 65 Carrasco-Chinchilla F, Muñoz-García AJ, Domínguez-Franco A. , et al. Remote ischaemic postconditioning: does it protect against ischaemic damage in percutaneous coronary revascularisation? Randomised placebo-controlled clinical trial. Heart 2013; 99 (19) 1431-1437
    CrossrefPubMedGoogle Scholar
  • 66 Luo SJ, Zhou YJ, Shi DM, Ge HL, Wang JL, Liu RF. Remote ischemic preconditioning reduces myocardial injury in patients undergoing coronary stent implantation. Can J Cardiol 2013; 29 (09) 1084-1089
    CrossrefPubMedGoogle Scholar
  • 67 Zografos TA, Katritsis GD, Tsiafoutis I, Bourboulis N, Katsivas A, Katritsis DG. Effect of one-cycle remote ischemic preconditioning to reduce myocardial injury during percutaneous coronary intervention. Am J Cardiol 2014; 113 (12) 2013-2017
    CrossrefPubMedGoogle Scholar
  • 68 Ghaemian A, Nouraei SM, Abdollahian F, Naghshvar F, Giussani DA, Nouraei SA. Remote ischemic preconditioning in percutaneous coronary revascularization: a double-blind randomized controlled clinical trial. Asian Cardiovasc Thorac Ann 2012; 20 (05) 548-554
    CrossrefPubMedGoogle Scholar
  • 69 Laiwalla AN, Ooi YC, Liou R, Gonzalez NR. Matched cohort analysis of the effects of limb remote ischemic conditioning in patients with aneurysmal subarachnoid hemorrhage. Transl Stroke Res 2016; 7 (01) 42-48
    CrossrefPubMedGoogle Scholar
  • 70 Gonzalez NR, Connolly M, Dusick JR, Bhakta H, Vespa P. Phase I clinical trial for the feasibility and safety of remote ischemic conditioning for aneurysmal subarachnoid hemorrhage. Neurosurgery 2014; 75 (05) 590-598 , discussion 598
    CrossrefPubMedGoogle Scholar
  • 71 Kim WH, Lee JH, Kim GS, Sim HY, Kim SJ. The effect of remote ischemic postconditioning on graft function in patients undergoing living donor kidney transplantation. Transplantation 2014; 98 (05) 529-536
    CrossrefPubMedGoogle Scholar
  • 72 Hu Q, Luo W, Huang L, Huang R, Chen R, Gao Y. Multiorgan protection of remote ischemic perconditioning in valve replacement surgery. J Surg Res 2016; 200 (01) 13-20
    CrossrefPubMedGoogle Scholar
  • 73 Pinaud F, Corbeau JJ, Baufreton C. , et al. Remote ischemic preconditioning in aortic valve surgery: Results of a randomized controlled study. J Cardiol 2016; 67 (01) 36-41
    CrossrefPubMedGoogle Scholar
  • 74 Holmberg FE, Ottas KA, Andreasen C. , et al. Conditioning techniques and ischemic reperfusion injury in relation to on-pump cardiac surgery. Scand Cardiovasc J 2014; 48 (04) 241-248
    CrossrefPubMedGoogle Scholar
  • 75 Lomivorotov VV, Shmyrev VA, Nepomnyaschih VA. , et al. Remote ischaemic preconditioning does not protect the heart in patients undergoing coronary artery bypass grafting. Interact Cardiovasc Thorac Surg 2012; 15 (01) 18-22
    CrossrefPubMedGoogle Scholar
  • 76 Choi YS, Shim JK, Kim JC. , et al. Effect of remote ischemic preconditioning on renal dysfunction after complex valvular heart surgery: a randomized controlled trial. J Thorac Cardiovasc Surg 2011; 142 (01) 148-154
    CrossrefPubMedGoogle Scholar
  • 77 Li L, Luo W, Huang L. , et al. Remote perconditioning reduces myocardial injury in adult valve replacement: a randomized controlled trial. J Surg Res 2010; 164 (01) e21-e26
    CrossrefPubMedGoogle Scholar
  • 78 Mayor F, Bilgin-Freiert A, Connolly M. , et al. Effects of remote ischemic preconditioning on the coagulation profile of patients with aneurysmal subarachnoid hemorrhage: a case-control study. Neurosurgery 2013; 73 (05) 808-815 , discussion 815
    CrossrefPubMedGoogle Scholar
  • 79 Hepponstall M, Ignjatovic V, Binos S. , et al. Remote ischemic preconditioning (RIPC) modifies the plasma proteome in children undergoing repair of tetralogy of fallot: a randomized controlled trial. PLoS One 2015; 10 (03) e0122778
    CrossrefPubMedGoogle Scholar
  • 80 Thygesen K, Alpert JS, White HD. , et al; Joint ESC/ACCF/AHA/WHF Task Force for the Redefinition of Myocardial Infarction. Universal definition of myocardial infarction. Circulation 2007; 116 (22) 2634-2653
    CrossrefPubMedGoogle Scholar
  • 81 Thygesen K, Alpert JS, Jaffe AS. , et al; Joint ESC/ACCF/AHA/WHF Task Force for the Universal Definition of Myocardial Infarction. Third universal definition of myocardial infarction. Circulation 2012; 126 (16) 2020-2035
    CrossrefPubMedGoogle Scholar
  • 82 Lanza GA, Stazi A, Villano A. , et al. Effect of remote ischemic preconditioning on platelet activation induced by coronary procedures. Am J Cardiol 2016; 117 (03) 359-365
    CrossrefPubMedGoogle Scholar
  • 83 Stazi A, Scalone G, Laurito M. , et al. Effect of remote ischemic preconditioning on platelet activation and reactivity induced by ablation for atrial fibrillation. Circulation 2014; 129 (01) 11-17
    CrossrefPubMedGoogle Scholar
  • 84 Massberg S, Enders G, Leiderer R. , et al. Platelet-endothelial cell interactions during ischemia/reperfusion: the role of P-selectin. Blood 1998; 92 (02) 507-515
    PubMedGoogle Scholar
  • 85 Hjortdal VE, Sinclair T, Kerrigan CL, Solymoss S. Arterial ischemia in skin flaps: microcirculatory intravascular thrombosis. Plast Reconstr Surg 1994; 93 (02) 375-385
    CrossrefPubMedGoogle Scholar
  • 86 Choukér A, Martignoni A, Schauer RJ. , et al. Alpha-gluthathione S-transferase as an early marker of hepatic ischemia/reperfusion injury after liver resection. World J Surg 2005; 29 (04) 528-534
    CrossrefPubMedGoogle Scholar
  • 87 Khalili H, Patel VG, Mayo HG. , et al. Surrogate and clinical outcomes following ischemic postconditioning during primary percutaneous coronary intervention of ST--segment elevation myocardial infarction: a meta-analysis of 15 randomized trials. Catheter Cardiovasc Interv 2014; 84 (06) 978-986
    CrossrefPubMedGoogle Scholar
  • 88 Hu XQ, Cheng J, Tang B. , et al. Clinical effect of postconditioning in ST-elevation myocardial infarction patients treated with primary percutaneous coronary intervention: a meta-analysis of randomized controlled trials. J Zhejiang Univ Sci B 2015; 16 (03) 198-207
    CrossrefPubMedGoogle Scholar
  • 89 Deng QW, Xia ZQ, Qiu YX. , et al. Clinical benefits of aortic cross-clamping versus limb remote ischemic preconditioning in coronary artery bypass grafting with cardiopulmonary bypass: a meta-analysis of randomized controlled trials. J Surg Res 2015; 193 (01) 52-68
    CrossrefPubMedGoogle Scholar
  • 90 Chai Q, Liu J. Early stage effect of ischemic preconditioning for patients undergoing on-pump coronary artery bypass grafts surgery: systematic review and meta-analysis. Pak J Med Sci 2014; 30 (03) 642-648
    PubMedGoogle Scholar
  • 91 Simillis C, Robertson FP, Afxentiou T, Davidson BR, Gurusamy KS. A network meta-analysis comparing perioperative outcomes of interventions aiming to decrease ischemia reperfusion injury during elective liver resection. Surgery 2016; 159 (04) 1157-1169
    CrossrefPubMedGoogle Scholar
  • 92 Rahbari NN, Wente MN, Schemmer P. , et al. Systematic review and meta-analysis of the effect of portal triad clamping on outcome after hepatic resection. Br J Surg 2008; 95 (04) 424-432
    CrossrefPubMedGoogle Scholar
  • 93 King N, Dieberg G, Smart NA. Effects of pre-procedural remote ischaemic pre-conditioning on the outcomes of elective percutaneous coronary intervention. A systematic review and meta-analysis. Clin Trials Regul Sci Cardiol 2016; 21: 1-6
    PubMedGoogle Scholar
  • 94 Pei H, Wu Y, Wei Y, Yang Y, Teng S, Zhang H. Remote ischemic preconditioning reduces perioperative cardiac and renal events in patients undergoing elective coronary intervention: a meta-analysis of 11 randomized trials. PLoS One 2014; 9 (12) e115500
    CrossrefPubMedGoogle Scholar
  • 95 Sardar P, Chatterjee S, Kundu A. , et al. Remote ischemic preconditioning in patients undergoing cardiovascular surgery: evidence from a meta-analysis of randomized controlled trials. Int J Cardiol 2016; 221: 34-41
    CrossrefPubMedGoogle Scholar
  • 96 Healy DA, Khan WA, Wong CS. , et al; Remote Preconditioning Trialists' Group. Remote preconditioning and major clinical complications following adult cardiovascular surgery: systematic review and meta-analysis. Int J Cardiol 2014; 176 (01) 20-31
    CrossrefPubMedGoogle Scholar
  • 97 Brevoord D, Kranke P, Kuijpers M, Weber N, Hollmann M, Preckel B. Remote ischemic conditioning to protect against ischemia-reperfusion injury: a systematic review and meta-analysis. PLoS One 2012; 7 (07) e42179
    CrossrefPubMedGoogle Scholar
  • 98 Wendel HP, Scholpp J, Schulze HJ, Heller W, Schwenzer N. Evaluation of markers of deep vein thrombosis in patients undergoing surgery for maxillofacial malignancies. J Craniomaxillofac Surg 1999; 27 (04) 266-270
    CrossrefPubMedGoogle Scholar
  • 99 Olsson E, Svartling N, Asko-Seljavaara S, Lassila R. Activation of coagulation and fibrinolysis during reconstructive microsurgery in patients with cancer. Microsurgery 2001; 21 (05) 208-213
    CrossrefPubMedGoogle Scholar
  • 100 Kakei Y, Akashi M, Hasegawa T, Minamikawa T, Usami S, Komori T. Incidence of venous thromboembolism after oral oncologic surgery with simultaneous reconstruction. J Oral Maxillofac Surg 2016; 74 (01) 212-217
    CrossrefPubMedGoogle Scholar
  • 101 Chaput B, Vergez S, Somda S. , et al. Comparison of single and double venous anastomoses in head and neck oncologic reconstruction using free flaps: A meta-analysis. Plast Reconstr Surg 2016; 137 (05) 1583-1594
    CrossrefPubMedGoogle Scholar