The no-reflow phenomenon: State of the art

Archives of Cardiovascular Diseases

Volumn 108, Issue 12, 2015, Pages 661-674

  Bouleti, Claire ^a,b,c,d,e   Mewton, Nathan ^e,f   Germain, Stéphane ^c,d,e  

^a BICHAT HOSPITAL   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d CNRS   (France)

^e INSERM   (France)

^f LOUIS PRADEL HOSPITAL   (France)

Author keywords

angioplasty; Ischaemia; No reflow; Primary coronary; Reperfusion; Vascular permeability

Indexed keywords

ABCIXIMAB; ADENOSINE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; ANGIOPOIETIN 1; ANGIOPOIETIN LIKE 4; ANTITHROMBOCYTIC AGENT; CD11B ANTIGEN; CLOPIDOGREL; CYCLOSPORIN A; CYTOCHROME C; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GADOLINIUM; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; METOPROLOL; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NICARDIPINE; NITROPRUSSIDE SODIUM; P SELECTIN GLYCOPROTEIN LIGAND 1; PADGEM PROTEIN; PLACEBO; PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; VERAPAMIL;

ACUTE HEART INFARCTION; APOPTOSIS; BLEEDING; BLOOD VESSEL INJURY; BLOOD VESSEL PERMEABILITY; CARDIOVASCULAR MAGNETIC RESONANCE; CELL DEATH; CONTRAST ENHANCEMENT; CORONARY ARTERY ATHEROSCLEROSIS; CORONARY BLOOD VESSEL; DRUG EFFICACY; EDEMA; EMBOLIC PROTECTION FILTER; EMBOLISM; ENDOTHELIUM; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; GRAFT PATENCY; HEART; HEART INFARCTION SIZE; HEART MUSCLE BLOOD FLOW; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; HUMAN; INFLAMMATION; ISCHEMIC POSTCONDITIONING; MEDICAL RESEARCH; META ANALYSIS (TOPIC); MICROTHROMBUS; MICROVASCULATURE; NEUTROPHIL CHEMOTAXIS; NO REFLOW PHENOMENON; NONHUMAN; PATHOPHYSIOLOGY; PERCUTANEOUS CORONARY INTERVENTION; PHASE 2 CLINICAL TRIAL (TOPIC); PREDICTIVE VALUE; PROGNOSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); REPERFUSION INJURY; REVIEW; SENSITIVITY AND SPECIFICITY; ST SEGMENT ELEVATION MYOCARDIAL INFARCTION; THROMBUS ASPIRATION; TRANSTHORACIC ECHOCARDIOGRAPHY; TREATMENT FAILURE; VASCULAR ENDOTHELIUM; VASOCONSTRICTION; COMPLICATION; CORONARY ARTERY BLOOD FLOW; ELECTROCARDIOGRAPHY; MYOCARDIAL INFARCTION; NO-REFLOW PHENOMENON; PHYSIOLOGY; PROCEDURES;

CORONARY CIRCULATION; CORONARY VESSELS; ELECTROCARDIOGRAPHY; HUMANS; MYOCARDIAL INFARCTION; NO-REFLOW PHENOMENON; PERCUTANEOUS CORONARY INTERVENTION; PROGNOSIS;

EID: 84947967372     PISSN: 18752136     EISSN: 18752128     Source Type: Journal    
DOI: 10.1016/j.acvd.2015.09.006     Document Type: Review

References (137)

1. G. Guarini, A. Huqi, D. Morrone, P. Capozza, G. Todiere, and M. Marzilli Pharmacological approaches to coronary microvascular dysfunction Pharmacol Ther 144 2014 283 302
2. C.M. Gibson, and A. Schomig Coronary and myocardial angiography: angiographic assessment of both epicardial and myocardial perfusion Circulation 109 2004 3096 3105
3. I. Morishima, T. Sone, S. Mokuno, and et al. Clinical significance of no-reflow phenomenon observed on angiography after successful treatment of acute myocardial infarction with percutaneous transluminal coronary angioplasty Am Heart J 130 1995 239 243
4. G. Niccoli, F. Burzotta, L. Galiuto, and F. Crea Myocardial no-reflow in humans J Am Coll Cardiol 54 2009 281 292
5. S.H. Rezkalla, and R.A. Kloner Coronary no-reflow phenomenon: from the experimental laboratory to the cardiac catheterization laboratory Catheter Cardiovasc Interv 72 2008 950 957
6. H. Ito No-reflow phenomenon and prognosis in patients with acute myocardial infarction Nat Clin Pract Cardiovasc Med 3 2006 499 506
7. G. Niccoli, R.K. Kharbanda, F. Crea, and A.P. Banning No-reflow: again prevention is better than treatment Eur Heart J 31 2010 2449 2455
8. B.G. Schwartz, and R.A. Kloner Coronary no reflow J Mol Cell Cardiol 52 2012 873 882
9. R. Berg, and C. Buhari Treating and preventing no reflow in the cardiac catheterization laboratory Curr Cardiol Rev 8 2012 209 214
10. G. Heusch Cardioprotection: chances and challenges of its translation to the clinic Lancet 381 2013 166 175
11. G.M. Santoro, R. Valenti, P. Buonamici, and et al. Relation between ST-segment changes and myocardial perfusion evaluated by myocardial contrast echocardiography in patients with acute myocardial infarction treated with direct angioplasty Am J Cardiol 82 1998 932 937
12. J.P. Henriques, F. Zijlstra, A.W. van't Hof, and et al. Angiographic assessment of reperfusion in acute myocardial infarction by myocardial blush grade Circulation 107 2003 2115 2119
13. S. Hamada, T. Nishiue, S. Nakamura, and et al. TIMI frame count immediately after primary coronary angioplasty as a predictor of functional recovery in patients with TIMI 3 reperfused acute myocardial infarction J Am Coll Cardiol 38 2001 666 671
14. L. Galiuto, A. Lombardo, A. Maseri, and et al. Temporal evolution and functional outcome of no reflow: sustained and spontaneously reversible patterns following successful coronary recanalisation Heart 89 2003 731 737
15. H. Ito, A. Maruyama, K. Iwakura, and et al. Clinical implications of the 'no reflow' phenomenon. A predictor of complications and left ventricular remodeling in reperfused anterior wall myocardial infarction Circulation 93 1996 223 228
16. K.C. Wu, E.A. Zerhouni, R.M. Judd, and et al. Prognostic significance of microvascular obstruction by magnetic resonance imaging in patients with acute myocardial infarction Circulation 97 1998 765 772
17. A.J. Taylor, N. Al-Saadi, H. Abdel-Aty, J. Schulz-Menger, D.R. Messroghli, and M.G. Friedrich Detection of acutely impaired microvascular reperfusion after infarct angioplasty with magnetic resonance imaging Circulation 109 2004 2080 2085
18. I. Eitel, S. de Waha, J. Wohrle, and et al. Comprehensive prognosis assessment by CMR imaging after ST-segment elevation myocardial infarction J Am Coll Cardiol 64 2014 1217 1226
19. V. Hombach, O. Grebe, N. Merkle, and et al. Sequelae of acute myocardial infarction regarding cardiac structure and function and their prognostic significance as assessed by magnetic resonance imaging Eur Heart J 26 2005 549 557
20. I. Morishima, T. Sone, K. Okumura, and et al. Angiographic no-reflow phenomenon as a predictor of adverse long-term outcome in patients treated with percutaneous transluminal coronary angioplasty for first acute myocardial infarction J Am Coll Cardiol 36 2000 1202 1209
21. F.S. Resnic, M. Wainstein, M.K. Lee, and et al. No-reflow is an independent predictor of death and myocardial infarction after percutaneous coronary intervention Am Heart J 145 2003 42 46
22. H. Ito Etiology and clinical implications of microvascular dysfunction in patients with acute myocardial infarction Int Heart J 55 2014 185 189
23. T. Reffelmann, and R.A. Kloner Microvascular reperfusion injury: rapid expansion of anatomic no reflow during reperfusion in the rabbit Am J Physiol Heart Circ Physiol 283 2002 H1099 H1107
24. A. Abbate, M.C. Kontos, and G.G. Biondi-Zoccai No-reflow: the next challenge in treatment of ST-elevation acute myocardial infarction Eur Heart J 29 2008 1795 1797
25. R.A. Kloner, C.E. Ganote, and R.B. Jennings The "no-reflow" phenomenon after temporary coronary occlusion in the dog J Clin Invest 54 1974 1496 1508
26. J. Tranum-Jensen, M.J. Janse, W.T. Fiolet, W.J. Krieger, C.N. D'Alnoncourt, and D. Durrer Tissue osmolality, cell swelling, and reperfusion in acute regional myocardial ischemia in the isolated porcine heart Circ Res 49 1981 364 381
27. A. Durante, and P.G. Camici Novel insights into an "old" phenomenon: the no reflow Int J Cardiol 187 2015 273 280
28. R.A. Kloner, R.E. Rude, N. Carlson, P.R. Maroko, L.W. DeBoer, and E. Braunwald Ultrastructural evidence of microvascular damage and myocardial cell injury after coronary artery occlusion: which comes first? Circulation 62 1980 945 952
29. R. Bolli, M.O. Jeroudi, B.S. Patel, and et al. Direct evidence that oxygen-derived free radicals contribute to postischemic myocardial dysfunction in the intact dog Proc Natl Acad Sci USA 86 1989 4695 4699
30. R.L. Engler, G.W. Schmid-Schonbein, and R.S. Pavelec Leukocyte capillary plugging in myocardial ischemia and reperfusion in the dog Am J Pathol 111 1983 98 111
31. G. Ambrosio, and I. Tritto Reperfusion injury: experimental evidence and clinical implications Am Heart J 138 1999 S69 S75
32. H. el-Tamimi, G.J. Davies, P. Sritara, D. Hackett, F. Crea, and A. Maseri Inappropriate constriction of small coronary vessels as a possible cause of a positive exercise test early after successful coronary angioplasty Circulation 84 1991 2307 2312
33. G. Ambrosio, H.F. Weisman, J.A. Mannisi, and L.C. Becker Progressive impairment of regional myocardial perfusion after initial restoration of postischemic blood flow Circulation 80 1989 1846 1861
34. T. Reffelmann, S.L. Hale, G. Li, and R.A. Kloner Relationship between no reflow and infarct size as influenced by the duration of ischemia and reperfusion Am J Physiol Heart Circ Physiol 282 2002 H766 H772
35. G. Ndrepepa, K. Tiroch, D. Keta, and et al. Predictive factors and impact of no reflow after primary percutaneous coronary intervention in patients with acute myocardial infarction Circ Cardiovasc Interv 3 2010 27 33
36. C. Bouleti, T. Mathivet, J.M. Serfaty, and et al. Angiopoietin-like 4 serum levels on admission for acute myocardial infarction are associated with no-reflow Int J Cardiol 187 2015 511 516
37. K. Iwakura, H. Ito, S. Kawano, and et al. Predictive factors for development of the no-reflow phenomenon in patients with reperfused anterior wall acute myocardial infarction J Am Coll Cardiol 38 2001 472 477
38. G. Niccoli, G.A. Lanza, S. Shaw, and et al. Endothelin-1 and acute myocardial infarction: a no-reflow mediator after successful percutaneous myocardial revascularization Eur Heart J 27 2006 1793 1798
39. B.K. Nallamothu, E.H. Bradley, and H.M. Krumholz Time to treatment in primary percutaneous coronary intervention N Engl J Med 357 2007 1631 1638
40. H.F. Dvorak Discovery of vascular permeability factor (VPF) Exp Cell Res 312 2006 522 526
41. A. Kawamoto, H. Kawata, Y. Akai, and et al. Serum levels of VEGF and basic FGF in the subacute phase of myocardial infarction Int J Cardiol 67 1998 47 54
42. Y. Hojo, U. Ikeda, Y. Zhu, and et al. Expression of vascular endothelial growth factor in patients with acute myocardial infarction J Am Coll Cardiol 35 2000 968 973
43. A. Kranz, C. Rau, M. Kochs, and J. Waltenberger Elevation of vascular endothelial growth factor-A serum levels following acute myocardial infarction. Evidence for its origin and functional significance J Mol Cell Cardiol 32 2000 65 72
44. Y. Sasaki, A. Kawamoto, M. Iwano, and et al. Vascular endothelial growth factor mRNA synthesis by peripheral blood mononuclear cells in patients with acute myocardial infarction Int J Cardiol 81 2001 51 60
45. X. Xu, J. Li, M. Simons, J. Li, R.J. Laham, and F.W. Sellke Expression of vascular endothelial growth factor and its receptors is increased, but microvascular relaxation is impaired in patients after acute myocardial ischemia J Thorac Cardiovasc Surg 121 2001 735 742
46. K. Korybalska, M. Pyda, E. Kawka, S. Grajek, A. Breborowicz, and J. Witowski Interpretation of elevated serum VEGF concentrations in patients with myocardial infarction Cytokine 54 2011 74 78
47. A. Taddei, C. Giampietro, A. Conti, and et al. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5 Nat Cell Biol 10 2008 923 934
48. S.M. Weis, and D.A. Cheresh Pathophysiological consequences of VEGF-induced vascular permeability Nature 437 2005 497 504
49. F. Orsenigo, C. Giampietro, A. Ferrari, and et al. Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo Nat Commun 3 2012 1208
50. R. Jaffe, A. Dick, and B.H. Strauss Prevention and treatment of microvascular obstruction-related myocardial injury and coronary no-reflow following percutaneous coronary intervention: a systematic approach JACC Cardiovasc Interv 3 2010 695 704
51. A. Tanaka, T. Kawarabayashi, Y. Nishibori, and et al. No-reflow phenomenon and lesion morphology in patients with acute myocardial infarction Circulation 105 2002 2148 2152
52. A. Okamura, H. Ito, K. Iwakura, and et al. Detection of embolic particles with the Doppler guide wire during coronary intervention in patients with acute myocardial infarction: efficacy of distal protection device J Am Coll Cardiol 45 2005 212 215
53. A. Skyschally, K. Leineweber, P. Gres, M. Haude, R. Erbel, and G. Heusch Coronary microembolization Basic Res Cardiol 101 2006 373 382
54. E.J. Topol, and J.S. Yadav Recognition of the importance of embolization in atherosclerotic vascular disease Circulation 101 2000 570 580
55. C. Cavallini, S. Savonitto, R. Violini, and et al. Impact of the elevation of biochemical markers of myocardial damage on long-term mortality after percutaneous coronary intervention: results of the CK-MB and PCI study Eur Heart J 26 2005 1494 1498
56. A. Skyschally, B. Walter, and G. Heusch Coronary microembolization during early reperfusion: infarct extension, but protection by ischaemic postconditioning Eur Heart J 34 2013 3314 3321
57. O. Frobert, B. Lagerqvist, G.K. Olivecrona, and et al. Thrombus aspiration during ST-segment elevation myocardial infarction N Engl J Med 369 2013 1587 1597
58. S.S. Jolly, J.A. Cairns, S. Yusuf, and et al. Randomized trial of primary PCI with or without routine manual thrombectomy N Engl J Med 372 2015 1389 1398
59. R. Nijveldt, A.M. Beek, A. Hirsch, and et al. Functional recovery after acute myocardial infarction: comparison between angiography, electrocardiography, and cardiovascular magnetic resonance measures of microvascular injury J Am Coll Cardiol 52 2008 181 189
60. G. Ndrepepa, K. Tiroch, M. Fusaro, and et al. 5-year prognostic value of no-reflow phenomenon after percutaneous coronary intervention in patients with acute myocardial infarction J Am Coll Cardiol 55 2010 2383 2389
61. C.E. Rochitte, J.A. Lima, D.A. Bluemke, and et al. Magnitude and time course of microvascular obstruction and tissue injury after acute myocardial infarction Circulation 98 1998 1006 1014
62. A.W. van't Hof The thrombolysis in myocardial infarction (TIMI) trial. Phase I findings. TIMI Study Group N Engl J Med 312 1985 932 936
63. I. Eitel, J. Wohrle, H. Suenkel, and et al. Intracoronary compared with intravenous bolus abciximab application during primary percutaneous coronary intervention in ST-segment elevation myocardial infarction: cardiac magnetic resonance substudy of the AIDA STEMI trial J Am Coll Cardiol 61 2013 1447 1454
64. A.W. van't Hof, A. Liem, H. Suryapranata, J.C. Hoorntje, M.J. de Boer, and F. Zijlstra Angiographic assessment of myocardial reperfusion in patients treated with primary angioplasty for acute myocardial infarction: myocardial blush grade. Zwolle Myocardial Infarction Study Group Circulation 97 1998 2302 2306
65. J. Vicente, N. Mewton, P. Croisille, and et al. Comparison of the angiographic myocardial blush grade with delayed-enhanced cardiac magnetic resonance for the assessment of microvascular obstruction in acute myocardial infarctions Catheter Cardiovasc Interv 74 2009 1000 1007
66. R. Nijveldt, P.A. van der Vleuten, A. Hirsch, and et al. Early electrocardiographic findings and MR imaging-verified microvascular injury and myocardial infarct size JACC Cardiovasc Imaging 2 2009 1187 1194
67. R. Nijveldt, M.B. Hofman, A. Hirsch, and et al. Assessment of microvascular obstruction and prediction of short-term remodeling after acute myocardial infarction: cardiac MR imaging study Radiology 250 2009 363 370
68. T.S. Albert, R.J. Kim, and R.M. Judd Assessment of no-reflow regions using cardiac MRI Basic Res Cardiol 101 2006 383 390
69. P. Croisille, D. Revel, and M. Saeed Contrast agents and cardiac MR imaging of myocardial ischemia: from bench to bedside Eur Radiol 16 2006 1951 1963
70. D. Garcia-Dorado, J. Oliveras, J. Gili, and et al. Analysis of myocardial oedema by magnetic resonance imaging early after coronary artery occlusion with or without reperfusion Cardiovasc Res 27 1993 1462 1469
71. J. Ganame, G. Messalli, S. Dymarkowski, and et al. Impact of myocardial haemorrhage on left ventricular function and remodelling in patients with reperfused acute myocardial infarction Eur Heart J 30 2009 1440 1449
72. K.C. Wu, R.J. Kim, D.A. Bluemke, and et al. Quantification and time course of microvascular obstruction by contrast-enhanced echocardiography and magnetic resonance imaging following acute myocardial infarction and reperfusion J Am Coll Cardiol 32 1998 1756 1764
73. M. Viallon, A. Jacquier, C. Rotaru, and et al. Head-to-head comparison of eight late gadolinium-enhanced cardiac MR (LGE CMR) sequences at 1.5 tesla: from bench to bedside J Magn Reson Imaging 34 2011 1374 1387
74. M. van Kranenburg, M. Magro, H. Thiele, and et al. Prognostic value of microvascular obstruction and infarct size, as measured by CMR in STEMI patients JACC Cardiovasc Imaging 7 2014 930 939
75. N. Mewton, S. Rapacchi, L. Augeul, and et al. Determination of the myocardial area at risk with pre-versus post-reperfusion imaging techniques in the pig model Basic Res Cardiol 106 2011 1247 1257
76. L.F. Robbers, E.S. Eerenberg, P.F. Teunissen, and et al. Magnetic resonance imaging-defined areas of microvascular obstruction after acute myocardial infarction represent microvascular destruction and haemorrhage Eur Heart J 34 2013 2346 2353
77. F. Bonner, M.W. Merx, K. Klingel, and et al. Monocyte imaging after myocardial infarction with 19F MRI at 3T: a pilot study in explanted porcine hearts Eur Heart J Cardiovasc Imaging 16 6 2015 612 620
78. J.F. Beltrame, F. Crea, and P. Camici Advances in coronary microvascular dysfunction Heart Lung Circ 18 2009 19 27
79. A. Kurtul, M. Yarlioglues, S.N. Murat, and et al. Usefulness of the platelet-to-lymphocyte ratio in predicting angiographic reflow after primary percutaneous coronary intervention in patients with acute ST-segment elevation myocardial infarction Am J Cardiol 114 2014 342 347
80. B. Ibanez, G. Heusch, M. Ovize, and F. Van de Werf Evolving therapies for myocardial ischemia/reperfusion injury J Am Coll Cardiol 65 2015 1454 1471
81. Z.Q. Zhao, J.S. Corvera, M.E. Halkos, and et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning Am J Physiol Heart Circ Physiol 285 2003 H579 H588
82. Z.Q. Zhao, C.D. Morris, J.M. Budde, and et al. Inhibition of myocardial apoptosis reduces infarct size and improves regional contractile dysfunction during reperfusion Cardiovasc Res 59 2003 132 142
83. P. Staat, G. Rioufol, C. Piot, and et al. Postconditioning the human heart Circulation 112 2005 2143 2148
84. N. Mewton, H. Thibault, F. Roubille, and et al. Postconditioning attenuates no-reflow in STEMI patients Basic Res Cardiol 108 2013 383
85. X. Freixa, N. Bellera, J.T. Ortiz-Perez, and et al. Ischaemic postconditioning revisited: lack of effects on infarct size following primary percutaneous coronary intervention Eur Heart J 33 2012 103 112
86. J.Y. Hahn, Y.B. Song, E.K. Kim, and 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 128 2013 1889 1896
87. C. Touboul, D. Angoulvant, N. Mewton, and et al. Ischaemic postconditioning reduces infarct size: systematic review and meta-analysis of randomized controlled trials Arch Cardiovasc Dis 108 2015 39 49
88. M. Ovize, G.F. Baxter, F. Di Lisa, and et al. Postconditioning and protection from reperfusion injury: where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology Cardiovasc Res 87 2010 406 423
89. S. Le Page, T. Bejan-Angoulvant, D. Angoulvant, and F. Prunier Remote ischemic conditioning and cardioprotection: a systematic review and meta-analysis of randomized clinical trials Basic Res Cardiol 110 2015 11
90. P.J. Vlaar, T. Svilaas, I.C. van der Horst, and et al. Cardiac death and reinfarction after 1 year in the thrombus aspiration during percutaneous coronary intervention in acute myocardial infarction study (TAPAS): a 1-year follow-up study Lancet 371 2008 1915 1920
91. F.P. Mongeon, P. Belisle, L. Joseph, M.J. Eisenberg, and S. Rinfret Adjunctive thrombectomy for acute myocardial infarction: a bayesian meta-analysis Circ Cardiovasc Interv 3 2010 6 16
92. A.A. Bavry, D.J. Kumbhani, and D.L. Bhatt Role of adjunctive thrombectomy and embolic protection devices in acute myocardial infarction: a comprehensive meta-analysis of randomized trials Eur Heart J 29 2008 2989 2990
93. F. Burzotta, M. De Vita, Y.L. Gu, and et al. Clinical impact of thrombectomy in acute ST-elevation myocardial infarction: an individual patient-data pooled analysis of 11 trials Eur Heart J 30 2009 2193 2203
94. G.W. Stone, J. Webb, D.A. Cox, and et al. Distal microcirculatory protection during percutaneous coronary intervention in acute ST-segment elevation myocardial infarction: a randomized controlled trial JAMA 293 2005 1063 1072
95. M. Gick, N. Jander, H.P. Bestehorn, and et al. Randomized evaluation of the effects of filter-based distal protection on myocardial perfusion and infarct size after primary percutaneous catheter intervention in myocardial infarction with and without ST-segment elevation Circulation 112 2005 1462 1469
96. J.D. Haeck, K.T. Koch, L. Bilodeau, and et al. Randomized comparison of primary percutaneous coronary intervention with combined proximal embolic protection and thrombus aspiration versus primary percutaneous coronary intervention alone in ST-segment elevation myocardial infarction: the PREPARE (PRoximal Embolic Protection in Acute myocardial infarction and Resolution of ST-Elevation) study JACC Cardiovasc Interv 2 2009 934 943
97. B. Ibanez, S. Prat-Gonzalez, W.S. Speidl, and et al. Early metoprolol administration before coronary reperfusion results in increased myocardial salvage: analysis of ischemic myocardium at risk using cardiac magnetic resonance Circulation 115 2007 2909 2916
98. B. Ibanez, G. Cimmino, S. Prat-Gonzalez, and et al. The cardioprotection granted by metoprolol is restricted to its administration prior to coronary reperfusion Int J Cardiol 147 2011 428 432
99. B. Ibanez, C. Macaya, V. Sanchez-Brunete, and et al. Effect of early metoprolol on infarct size in ST-segment-elevation myocardial infarction patients undergoing primary percutaneous coronary intervention: the effect of metoprolol in cardioprotection during an acute myocardial infarction (METOCARD-CNIC) trial Circulation 128 2013 1495 1503
100. G. Pizarro, L. Fernandez-Friera, V. Fuster, and et al. Long-term benefit of early pre-reperfusion metoprolol administration in patients with acute myocardial infarction: results from the METOCARD-CNIC trial (effect of metoprolol in cardioprotection during an acute myocardial infarction) J Am Coll Cardiol 63 2014 2356 2362
101. Z.M. Chen, H.C. Pan, Y.P. Chen, and et al. Early intravenous then oral metoprolol in 45,852 patients with acute myocardial infarction: randomised placebo-controlled trial Lancet 366 2005 1622 1632
102. D. Antoniucci Block the ischemia and reperfusion damage: an old adjunctive drug for a new reperfusion strategy J Am Coll Cardiol 63 2014 2363 2364
103. K.D. Garlid, P. Paucek, V. Yarov-Yarovoy, and et al. Cardioprotective effect of diazoxide and its interaction with mitochondrial ATP-sensitive K+ channels. Possible mechanism of cardioprotection Circ Res 81 1997 1072 1082
104. P. Korge, H.M. Honda, and J.N. Weiss Protection of cardiac mitochondria by diazoxide and protein kinase C: implications for ischemic preconditioning Proc Natl Acad Sci USA 99 2002 3312 3317
105. A. Micari, T.A. Belcik, E.A. Balcells, and et al. Improvement in microvascular reflow and reduction of infarct size with adenosine in patients undergoing primary coronary stenting Am J Cardiol 96 2005 1410 1415
106. M. Marzilli, E. Orsini, P. Marraccini, and R. Testa Beneficial effects of intracoronary adenosine as an adjunct to primary angioplasty in acute myocardial infarction Circulation 101 2000 2154 2159
107. K.W. Mahaffey, J.A. Puma, N.A. Barbagelata, and et al. Adenosine as an adjunct to thrombolytic therapy for acute myocardial infarction: results of a multicenter, randomized, placebo-controlled trial: the Acute Myocardial Infarction STudy of ADenosine (AMISTAD) Trial J Am Coll Cardiol 34 1999 1711 1720
108. M. Quintana, P. Hjemdahl, A. Sollevi, and et al. Left ventricular function and cardiovascular events following adjuvant therapy with adenosine in acute myocardial infarction treated with thrombolysis, results of the ATTenuation by Adenosine of Cardiac Complications (ATTACC) Study Eur J Clin Pharmacol 59 2003 1 9
109. A.M. Ross, R.J. Gibbons, G.W. Stone, R.A. Kloner, and R.W. Alexander A randomized, double-blinded, placebo-controlled multicenter trial of adenosine as an adjunct to reperfusion in the treatment of acute myocardial infarction (AMISTAD-II) J Am Coll Cardiol 45 2005 1775 1780
110. R.A. Kloner, M.B. Forman, R.J. Gibbons, A.M. Ross, R.W. Alexander, and G.W. Stone Impact of time to therapy and reperfusion modality on the efficacy of adenosine in acute myocardial infarction: the AMISTAD-2 trial Eur Heart J 27 2006 2400 2405
111. W. Desmet, J. Bogaert, C. Dubois, and et al. High-dose intracoronary adenosine for myocardial salvage in patients with acute ST-segment elevation myocardial infarction Eur Heart J 32 2011 867 877
112. D. Garcia-Dorado, B. Garcia-del-Blanco, I. Otaegui, and et al. Intracoronary injection of adenosine before reperfusion in patients with ST-segment elevation myocardial infarction: a randomized controlled clinical trial Int J Cardiol 177 2014 935 941
113. S.H. Rezkalla, K.C. Dharmashankar, I.B. Abdalrahman, and R.A. Kloner No-reflow phenomenon following percutaneous coronary intervention for acute myocardial infarction: incidence, outcome, and effect of pharmacologic therapy J Interv Cardiol 23 2010 429 436
114. Q. Su, L. Li, and Y. Liu Short-term effect of verapamil on coronary no-reflow associated with percutaneous coronary intervention in patients with acute coronary syndrome: a systematic review and meta-analysis of randomized controlled trials Clin Cardiol 36 2013 E11 E16
115. G. Amit, C. Cafri, S. Yaroslavtsev, and et al. Intracoronary nitroprusside for the prevention of the no-reflow phenomenon after primary percutaneous coronary intervention in acute myocardial infarction. A randomized, double-blind, placebo-controlled clinical trial Am Heart J 152 2006 887 e9-14
116. A. Zoni, P. Knoll, and T. Gherli Microvascular obstruction after successful fibrinolytic therapy in acute myocardial infarction. Comparison of reteplase vs reteplase + abciximab: a cardiovascular magnetic resonance study Heart Int 2 2006 54
117. G.W. Stone, A. Maehara, B. Witzenbichler, and et al. Intracoronary abciximab and aspiration thrombectomy in patients with large anterior myocardial infarction: the INFUSE-AMI randomized trial JAMA 307 2012 1817 1826
118. F. Roubille, O. Lairez, N. Mewton, and et al. Cardioprotection by clopidogrel in acute ST-elevated myocardial infarction patients: a retrospective analysis Basic Res Cardiol 107 2012 275
119. Task Force on the management of ST-segment elevation acute myocardial infarction of the European Society of Cardiology, P.G. Steg, S.K. James, and et al. ESC Guidelines for the management of acute myocardial infarction in patients presenting with ST-segment elevation Eur Heart J 33 2012 2569 2619
120. N. Mewton, F. Ivanes, M. Cour, and M. Ovize Postconditioning: from experimental proof to clinical concept Dis Model Mech 3 2010 39 44
121. N. Mewton, T. Bochaton, and M. Ovize Postconditioning the heart of ST-elevation myocardial infarction patients Circ J 77 2013 1123 1130
122. C. Piot, P. Croisille, P. Staat, and et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction N Engl J Med 359 2008 473 481
123. J. Zalewski, P. Claus, J. Bogaert, and et al. Cyclosporine A reduces microvascular obstruction and preserves left ventricular function deterioration following myocardial ischemia and reperfusion Basic Res Cardiol 110 2015 18
124. M. Mewton, T.T. Cung, O. Morel, and et al. Rationale and design of the Cyclosporine to ImpRove Clinical oUtcome in ST-elevation myocardial infarction patients (the CIRCUS trial) Am Heart J 169 6 2015 758-766.e6
125. G. Pannitteri, E. Petrucci, and U. Testa Coordinate release of angiogenic growth factors after acute myocardial infarction: evidence of a two-wave production J Cardiovasc Med (Hagerstown) 7 2006 872 879
126. A. Galaup, E. Gomez, R. Souktani, and et al. Protection against myocardial infarction and no-reflow through preservation of vascular integrity by angiopoietin-like 4 Circulation 125 2012 140 149
127. C. Bouleti, T. Mathivet, B. Coqueran, and et al. Protective effects of angiopoietin-like 4 on cerebrovascular and functional damages in ischaemic stroke Eur Heart J 34 2013 3657 3668
128. C. Bouleti, T. Mathivet, B. Lapergue, C. Monnot, and S. Germain [Protection of vascular integrity in reperfusion during stroke] Med Sci (Paris) 30 2014 608 610
129. J. Gavard, V. Patel, and J.S. Gutkind Angiopoietin-1 prevents VEGF-induced endothelial permeability by sequestering Src through mDia Dev Cell 14 2008 25 36
130. K. Hatanaka, A.A. Lanahan, M. Murakami, and M. Simons Fibroblast growth factor signaling potentiates VE-cadherin stability at adherens junctions by regulating SHP2 PLoS One 7 2012 e37600
131. R. Sandhu, K. Teichert-Kuliszewska, S. Nag, and et al. Reciprocal regulation of angiopoietin-1 and angiopoietin-2 following myocardial infarction in the rat Cardiovasc Res 64 2004 115 124
132. M. Murakami, L.T. Nguyen, Z.W. Zhuang, and et al. The FGF system has a key role in regulating vascular integrity J Clin Invest 118 2008 3355 3366
133. L. Eklund, and P. Saharinen Angiopoietin signaling in the vasculature Exp Cell Res 319 2013 1271 1280
134. R. Martinelli, M. Gegg, R. Longbottom, P. Adamson, P. Turowski, and J. Greenwood ICAM-1-mediated endothelial nitric oxide synthase activation via calcium and AMP-activated protein kinase is required for transendothelial lymphocyte migration Mol Biol Cell 20 2009 995 1000
135. P. He Leucocyte/endothelium interactions and microvessel permeability: coupled or uncoupled? Cardiovasc Res 87 2010 281 290
136. J. Aman, J. van Bezu, A. Damanafshan, and et al. Effective treatment of edema and endothelial barrier dysfunction with imatinib Circulation 126 2012 2728 2738
137. R.P. Betgem, G.A. de Waard, R. Nijveldt, A.M. Beek, J. Escaned, and N. van Royen Intramyocardial haemorrhage after acute myocardial infarction Nat Rev Cardiol 12 2015 156 167