The coronary circulation in cardioprotection: More than just one confounder

Cardiovascular Research

Volumn 94, Issue 2, 2012, Pages 237-245

  Heusch, Gerd ^a   Kleinbongard, Petra ^a   Skyschally, Andreas ^a   Levkau, Bodo ^a   Schulz, Rainer ^b   Erbel, Raimund ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Cardioprotection; Coronary blood flow; Infarct size; Myocardial ischaemia; Postconditioning; Preconditioning; Reperfusion

Indexed keywords

CREATINE KINASE; REACTIVE OXYGEN METABOLITE; SEROTONIN; THROMBOXANE; TROPONIN; TUMOR NECROSIS FACTOR ALPHA;

ATHEROSCLEROTIC PLAQUE; AUTOCRINE EFFECT; CORONARY ARTERY ATHEROSCLEROSIS; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY OBSTRUCTION; CORONARY ARTERY THROMBOSIS; CORONARY REPERFUSION; CREATINE KINASE BLOOD LEVEL; ELECTROCARDIOGRAM; GLYCOCALYX; HEART EDEMA; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; HYPEREMIA; MICROCIRCULATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PARACRINE SIGNALING; PERCUTANEOUS CORONARY INTERVENTION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REPERFUSION INJURY; REVIEW;

CORONARY CIRCULATION; HUMANS; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY;

EID: 84860162585     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr271     Document Type: Review

References (141)

1. Heusch G, Schulz R. Neglect of the coronary circulation: some critical remarks on problems in the translation of cardioprotection. Cardiovasc Res 2009;84:11-14.
2. Kleinbongard P, Konorza T, Böse D, Baars T, Haude M, Erbel R et al. Lessons from human coronary aspirate. J Mol Cell Cardiol 2011; doi:10.1016/j.yjmcc.2011.06.022.
3. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986;74:1124-1136. (Pubitemid 17174962)
4. Zhao Z-Q, Corvera JS, Halkos ME, Kerendi F,Wang N-P, Guyton RA et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 2003;285:H579-H588. (Pubitemid 36885888)
5. Przyklenk K, Bauer B, Ovize M, Kloner RA, Whittaker P. Regional ischemic 'preconditioning' protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation 1993;87:893-899. (Pubitemid 23070821)
6. Liu GS, Thornton J, van Winkle DM, Stanley AWH, Olsson RA, Downey JM. Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation 1991;84:350-356.
7. Ytrehus K, Liu Y, Downey JM. Preconditioning protects ischemic rabbit heart by protein C activation. Am J Physiol Heart Circ Physiol 1994;266:H1145-H1152. (Pubitemid 24121336)
8. Cohen MV, Downey JM. Cardioprotection: spotlight on PKG. Br J Pharmacol 2007; 152:833-834. (Pubitemid 350100495)
9. Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the reperfusion injury salvage kinase (RISK)-pathway. Cardiovasc Res 2004;61:448-460. (Pubitemid 38210151)
10. Lecour S. Multiple protective pathways against reperfusion injury: a SAFE path without Aktion? J Mol Cell Cardiol 2009;46:607-609.
11. Heusch G, Boengler K, Schulz R. Inhibition of mitochondrial permeability transition pore opening: the holy grail of cardioprotection. Basic Res Cardiol 2010;105: 151-154.
12. Heusch G, Boengler K, Schulz R. Cardioprotection: nitric oxide, protein kinases, and mitochondria. Circulation 2008;118:1915-1919.
13. Heusch G, Schulz R. Remote preconditioning. J Mol Cell Cardiol 2002;34:1279-1281. (Pubitemid 35244401)
14. Lim SY, Yellon DM, Hausenloy DJ. The neural and humoral pathways in remote limb ischemic preconditioning. Basic Res Cardiol 2010;105:651-655.
15. Yellon DM, Alkhulaifi AM, Pugsley WB. Preconditioning the human myocardium. Lancet 1993;342:276-277. (Pubitemid 23224422)
16. Staat P, Rioufol G, Piot C, Cottin Y, Cung TT, L'Huillier I et al. Postconditioning the human heart. Circulation 2005;112:2143-2148. (Pubitemid 41475808)
17. Hausenloy DJ, Mwamure PK, Venugopal V, Harris J, Barnard M, Grundy E et al. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomized controlled trial. Lancet 2007; 370:575-579. (Pubitemid 47247853)
18. Hausenloy DJ, Baxter G, Bell R, Botker HE, Davidson SM, Downey J et al. Translating novel strategies for cardioprotection: the Hatter Workshop Recommendations. Basic Res Cardiol 2010;105:677-686.
19. Ovize M, Baxter GF, Di Lisa F, Ferdinandy P, Garcia-Dorado D, Hausenloy DJ et al. Postconditioning and protection from reperfusion injury: where do we stand? Cardiovasc Res 2010;87:406-423.
20. Schwartz Longacre L, Kloner RA, Arai AE, Baines CP, Bolli R, Braunwald E et al. New horizons in cardioprotection: recommendations from the 2010 National Heart, Lung, and Blood Institute Workshop. Circulation 2011;124:1172-1179.
21. Boengler K, Schulz R, Heusch G. Loss of cardioprotection with ageing. Cardiovasc Res 2009;83:247-261.
22. Skyschally A, van Caster P, Iliodromitis EK, Schulz R, Kremastinos DT, Heusch G. Ischemic postconditioning-experimental models and protocol algorithms. Basic Res Cardiol 2009;104:469-483.
23. Heusch G. Reduction of infarct size by ischaemic post-conditioning in humans: fact or fiction? Eur Heart J 2011; doi:10.1093/eurheartj/ehr341.
24. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R. Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol 2010;30:1282-1292.
25. Ferrante G, Nakano M, Prati F, Niccoli G, Mallus MT, Ramazzotti V et al. High levels of systemic myeloperoxidase are associated with coronary plaque erosion in patients with acute coronary syndromes: a clinicopathological study. Circulation 2010;122:2505-2513.
26. Reimer KA, Lowe JE, Rasmussen MM, Jennings RB. The wavefront phenomenon of ischemic cell death. 1. Myocardial infarct size vs. duration of coronary occlusion in dogs. Circulation 1977;56:786-794. (Pubitemid 8235183)
27. Reimer KA, Jennings RB. The 'wavefront phenomenon' of myocardial ischemic cell death. II. Transmural progression of necrosis within the framework of ischemic bed size (myocardium at risk) and collateral flow. Lab Invest 1979;40:633-644. (Pubitemid 9191795)
28. Reimer KA, Jennings RB, Cobb FR, Murdock RH, Greenfield JC Jr, Becker LC et al. Animal models for protecting ischemic myocardium: results of the NHLBI cooperative study. Comparison of unconscious and conscious dog models. Circ Res 1985;56: 651-665. (Pubitemid 15093376)
29. Skyschally A, Schulz R, Heusch G. Pathophysiology of myocardial infarction: protection by ischemic pre-and postconditioning. Herz 2008;33:88-100. (Pubitemid 351437850)
30. Burns RJ, Gibbons RJ, Yi Q, Roberts RS, Miller TD, Schaer GL et al. The relationships of left ventricular ejection fraction, end-systolic volume index and infarct size to sixmonth mortality after hospital discharge following myocardial infarction treated by thrombolysis. J Am Coll Cardiol 2002;39:30-36. (Pubitemid 34059858)
31. Mahaffey KW, Puma JA, Barbagelata A, DiCarli MF, Leesar MA, Browne KF et al. Adenosine as an adjunct thrombolytic therapy for acute myocardial infarction. J Am Coll Cardiol 1999;34:1711-1720.
32. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 2008;359: 473-481.
33. Skyschally A, Leineweber K, Gres P, Haude M, Erbel R, Heusch G. Coronary microembolization. Basic Res Cardiol 2006;101:373-382. (Pubitemid 44275870)
34. Schulz R, Post H, Vahlhaus C, Heusch G. Ischemic preconditioning in pigs: a graded phenomenon. Its relation to adenosine and bradykinin. Circulation 1998;98: 1022-1029. (Pubitemid 28446656)
35. SchaperW. Collateral circulation: past and present. Basic Res Cardiol 2009;104:5-21.
36. Heusch G, Skyschally A, Schulz R. The in situ pig heart with regional ischemia/reperfusion-ready for translation. J Mol Cell Cardiol 2011;50:951-963.
37. Meier P, Gloekler S, Zbinden R, Beckh S, de Marchi SF, Zbinden S et al. Beneficial effect of recruitable collaterals: a 10-year follow-up study in patients with stable coronary artery disease undergoing quantitative collateral measurements. Circulation 2007;116:975-983. (Pubitemid 47329562)
38. Przyklenk K. Lethal myocardial 'reperfusion injury': the opinions of good men. J Thromb Thrombolysis 1997;4:5-6. (Pubitemid 27087181)
39. Heusch G. Postconditioning. Old wine in a new bottle? J Am Coll Cardiol 2004;44: 1111-1112. (Pubitemid 39165148)
40. Downey JM, Cohen MV. We think we see a pattern emerging here. Circulation 2005; 111:120-121. (Pubitemid 40139719)
41. Hausenloy DJ, Yellon DM. Preconditioning and postconditioning: united at reperfusion. Pharmacol Ther 2007;116:173-191. (Pubitemid 47451505)
42. Heusch G. Hibernating myocardium. Physiol Rev 1998;78:1055-1085. (Pubitemid 28491948)
43. Heusch G, Schulz R, Rahimtoola SH. Myocardial hibernation: a delicate balance. Am J Physiol Heart Circ Physiol 2005;288:H984-H999. (Pubitemid 40269997)
44. Page B, Young R, Iyer V, Suzuki G, Lis M, Korotchkina L et al. Persistent regional downregulation in mitochondrial enzymes and upregulation of stress proteins in swine with chronic hibernating myocardium. Circ Res 2008;102:103-112.
45. Shen YT, Depre C, Yan L, Park JY, Tian B, Jain K et al. Repetitive ischemia by coronary stenosis induces a novel window of ischemic preconditioning. Circulation 2008; 118:1961-1969.
46. Depre C, Park JY, Shen YT, Zhao X, Qiu H, Yan L et al. Molecular mechanisms mediating preconditioning following chronic ischemia differ from those in classical second window. Am J Physiol Heart Circ Physiol 2010;299:H752-H762.
47. Oikawa M, Yaoita H, Watanabe K, Maruyama Y. Attenuation of cardioprotective effect by postconditioning in coronary stenosed rat heart and its restoration by carvedilol. Circ J 2008;72:2081-2086.
48. Ovize M, Przyklenk K, Kloner RA. Partial coronary stenosis is sufficient and complete reperfusion is mandatory for preconditioning in the canine heart. Circ Res 1992;71:1165-1173.
49. Kapadia SJ, Terlato JS, Most AS. Presence of a critical coronary artery stenosis does not abolish the protective effect of ischemic preconditioning. Circulation 1997;95: 1286-1292. (Pubitemid 27097842)
50. Koning MMG, Simonis LAJ, deZeeuw S, Nieukoop S, Post S, Verdouw PD. Ischaemic preconditioning by partial occlusion without intermittent reperfusion. Cardiovasc Res 1994;28:1146-1151. (Pubitemid 24264718)
51. Schulz R, Post H, Sakka S, Wallbridge DR, Heusch G. Intraischemic preconditioning. Increased tolerance to sustained low-flow ischemia by a brief episode of no-flow ischemia without intermittent reperfusion. Circ Res 1995;76:942-950.
52. Bopassa JC, Michel P, Gateau-Roesch O, Ovize M, Ferrera R. Low-pressure reperfusion alters mitochondrial permeability transition. Am J Physiol Heart Circ Physiol 2005; 288:H2750-H2755. (Pubitemid 40720654)
53. Bopassa JC, Nemlin C, Sebbag L, Rodriguez C, Ovize M, Ferrera R. Optimal time duration for low-pressure controlled reperfusion to efficiently protect ischemic rat heart. Transplant Proc 2007;39:2615-2616. (Pubitemid 47588388)
54. Nemlin C, Benhabbouche S, Bopassa JC, Sebbag L, Ovize M, Ferrera R. Optimal pressure for low pressure controlled reperfusion to efficiently protect ischemic heart: an experimental study in rats. Transplant Proc 2009;41:703-704.
55. Okamoto F, Allen BS, Buckberg GD, Bugyi H, Leaf J. Studies of controlled reperfusion after ischemia. XIV. Reperfusion conditions: Importance of ensuring gentle versus sudden reperfusion during relief of coronary occlusion. J Thorac Cardiovasc Surg 1986;92:613-620. (Pubitemid 16020177)
56. Sato H, Jordan JE, Zhao Z-Q, Sarvotham SS, Vinten-Johansen J. Gradual reperfusion reduces infarct size and endothelial injury but augments neutrophil accumulation. Ann Thorac Surg 1997;64:1099-1107. (Pubitemid 27497391)
57. Granato JE, Watson DD, Flanagan TL, Beller GA. Myocardial thallium-201 kinetics and regional flow alterations with 3 h of coronary occlusion and either rapid reperfusion through a totally patent vessel or slow reperfusion through a critical stenosis. J Am Coll Cardiol 1987;9:109-118. (Pubitemid 17219554)
58. Musiolik J, van Caster P, Skyschally A, Boengler K, Gres P, Schulz R et al. Reduction of infarct size by gentle reperfusion without activation of reperfusion injury salvage kinases in pigs. Cardiovasc Res 2010;85:110-117.
59. Rodriguez-Sinovas A, Cabestrero A, Garcia Del BB, Inserte J, Garcia A, Garcia-Dorado D. Intracoronary acid infusion as an alternative to ischemic postconditioning in pigs. Basic Res Cardiol 2009;104:761-771.
60. Heusch G, Kleinbongard P, Böse D, Levkau B, Haude M, Schulz R et al. Coronary microembolization: from bedside to bench and back to bedside. Circulation 2009; 120:1822-1836.
61. Wallace TW, Abdullah SM, Drazner MH, Das SR, Khera A, McGuire DK et al. Prevalence and determinants of troponin T elevation in the general population. Circulation 2006;113:1958-1965.
62. Eggers KM, Lind L, Ahlstrom H, Bjerner T, Ebeling BC, Larsson A et al. Prevalence and pathophysiological mechanisms of elevated cardiac troponin I levels in a population-based sample of elderly subjects. Eur Heart J 2008;29:2252-2258.
63. Möhlenkamp S, Schmermund A, Lehmann N, Roggenbuck U, Dragano N, Stang A et al. Subclinical coronary atherosclerosis and resting ECG abnormalities in an unselected general population. Atherosclerosis 2008;196:786-794.
64. de Lemos JA, Drazner MH, Omland T, Ayers CR, Khera A, Rohatgi A et al. Association of troponin T detected with a highly sensitive assay and cardiac structure and mortality risk in the general population. JAMA 2010;304:2503-2512.
65. Kloner RA, Shook T, Przyklenk K, Davis VG, Junio L, Matthews RV et al. Previous angina alters in-hospital outcome in TIMI 4. A clinical correlate to preconditioning? Circulation 1995;91:37-47.
66. Ottani F, Galvani M, Ferrini D, Sorbello F, Limonetti P, Pantoli D et al. Prodromal angina limits infarct size. A role for ischemic preconditioning. Circulation 1995;91: 291-297.
67. Nakagawa Y, Ito H, Kitakaze M, Kusuoka H, Hori M, Kuzuya T et al. Effect of angina pectoris on myocardial protection in patients with reperfused anterior wall myocardial infarction: retrospective clinical evidence of 'preconditioning'. J Am Coll Cardiol 1995;25:1076-1083.
68. Kloner RA, Shook T, Antman EM, Cannon CP, Przyklenk K, Yoo K et al. Prospective temporal analysis of the onset of preinfarction angina versus outcome. An ancillary study in TIMI-9B. Circulation 1998;97:1042-1045.
69. Andreotti F, Pasceri V, Hackett DR, Davies GJ, Haider AW, Maseri A. Preinfarction as a predictor of more rapid coronary thrombolysis in patients with acute myocardial infarction. N Engl J Med 1996;334:7-12. (Pubitemid 26012497)
70. Heusch G. Nitroglycerin and delayed preconditioning in humans. Yet another new mechanism for an old drug? Circulation 2001;103:2876-2878. (Pubitemid 32578120)
71. Schulz R, Rose J, Post H, Heusch G. Involvement of endogenous adenosine in ischaemic preconditioning in swine. Pflügers Arch 1995;430:273-282.
72. Skyschally A, Schulz R, Gres P, Konietzka I, Martin C, Haude M et al. Coronary microembolization does not induce acute preconditioning against infarction in pigs-the role of adenosine. Cardiovasc Res 2004;63:313-322. (Pubitemid 38900845)
73. Skyschally A, Gres P, Heusch P, Martin C, Haude M, Erbel R et al. Preinfarction angina: no interference of coronary microembolization with acute ischemic preconditioning. J Mol Cell Cardiol 2005;39:355-361. (Pubitemid 40995025)
74. Dörge H, Schulz R, Belosjorow S, Post H, van de Sand A, Konietzka I et al. Coronary microembolization: the role of TNFa in contractile dysfunction. J Mol Cell Cardiol 2002;34:51-62. (Pubitemid 34146395)
75. Skyschally A, Gres P, Hoffmann S, Haude M, Erbel R, Schulz R et al. Bidirectional role of tumor necrosis factor-a in coronary microembolization: progressive contractile dysfunction versus delayed protection against infarction. Circ Res 2007;100:140-146. (Pubitemid 46066782)
76. Heusch P, Skyschally A, Leineweber K, Haude M, Erbel R, Heusch G. The interaction of coronary microembolization and ischemic preconditioning: a third window of cardioprotection through TNF-alpha. Arch Med Sci 2007;2:83-92. (Pubitemid 47241094)
77. Loubeyre C, Morice MC, Lefevre T, Piechaud JF, Louvard Y, Dumas P. A randomized comparison of direct stenting with conventional stent implantation in selected patients with acute myocardial infarction. J Am Coll Cardiol 2002;39:15-21. (Pubitemid 34059856)
78. Stone GW, Brodie BR, Griffin JJ, Costantini C, Morice MC, St Goar FG et al. Clinical and angiographic follow-up after primary stenting in acute myocardial infarction: the Primary Angioplasty in Myocardial Infarction (PAMI) stent pilot trial. Circulation 1999; 99:1548-1554. (Pubitemid 29152920)
79. Mehta RH, Harjai KJ, Cox DA, Stone GW, Brodie BR, Boura J et al. Comparison of coronary stenting versus conventional balloon angioplasty on five-year mortality in patients with acute myocardial infarction undergoing primary percutaneous coronary intervention. Am J Cardiol 2005;96:901-906. (Pubitemid 41362510)
80. Venugopal V, Hausenloy DJ, Ludman A, Di Salvo CM, Kolvekar S, Yap J et al. Remote ischaemic preconditioning reduces myocardial injury in patients undergoing cardiac surgery with cold blood cardioplegia: a randomised controlled trial. Heart 2009;95: 1567-1571.
81. Hoole SP, Heck PM, Sharples L, Khan SN, Duehmke R, Densem CG et al. Cardiac remote ischemic preconditioning in coronary stenting (CRISP Stent) study: a prospective, randomized control trial. Circulation 2009;119:820-827.
82. Munk K, Andersen NH, Schmidt MR, Nielsen SS, Terkelsen CJ, Sloth E et al. 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 2010;3: 656-662.
83. Rentoukas I, Giannopoulos G, Kaoukis A, Kossyvakis C, Raisakis K, Driva M et al. Cardioprotective role of remote ischemic periconditioning in primary percutaneous coronary intervention. JACC: Cardiovascular Interventions 2010;3:49-55.
84. Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, Peters J et al. Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass surgery with crystalloid cardioplegic arrest. Basic Res Cardiol 2010; 105:657-664.
85. Ku DD. Coronary vascular reactivity after acute myocardial ischemia. Science 1982; 218:576-578. (Pubitemid 12003044)
86. Bolli R, Triana JF, Jeroudi MO. Prolonged impairment of coronary vasodilation after reversible ischemia. Circ Res 1990;67:332-343.
87. Dauber IM, VanBenthuysen KM, McMurtry IF, Wheeler GS, Lesnefsky EJ, Horwitz LD et al. Functional coronary microvascular injury evident as increased permeability due to brief ischemia and reperfusion. Circ Res 1990;66:986-998. (Pubitemid 20126430)
88. Sellke FW, Quillen JE, Harrison DG. Effects of vasopressin on the coronary circulation following ischemia and reperfusion. Faseb J 1991;5(part II):A1387.
89. Gross GJ, O'Rourke ST, Pelc LR, Warltier DC. Myocardial and endothelial dysfunction after multiple, brief coronary occlusions: role of oxygene radicals. Am J Physiol 1992;263:H1703-H1709. (Pubitemid 23030721)
90. Ehring T, Krajcar M, Baumgart D, Kompa S, Hümmelgen M, Heusch G. Cholinergic and a-adrenergic coronary vasomotion with increasing ischemia-reperfusion injury. Am J Physiol 1995;268:H886-H894.
91. Kaeffer N, Richard V, Thuillez C. Delayed coronary endothelial protection 24 h after preconditioning role of free radicals. Circulation 1997;96:2311-2316.
92. Gewirtz H, Sasken H, Steiner M, Most AS. Impaired arteriolar vasodilation induced by thrombosis of a coronary arterial stenosis. Am J Physiol Heart Circ Physiol 1985;249: H1154-H1166. (Pubitemid 16171200)
93. Leineweber K, Böse D, Vogelsang M, Haude M, Erbel R, Heusch G. Intense vasoconstriction in response to aspirate from stented saphenous vein aortocoronary bypass grafts. J Am Coll Cardiol 2006;47:981-986.
94. Kleinbongard P, Böse D, Baars T, Möhlenkamp S, Konorza T, Schöner S et al. Vasoconstrictor potential of coronary aspirate from patients undergoing stenting of saphenous vein aortocoronary bypass grafts and its pharmacological attenuation. Circ Res 2011;108:344-352.
95. Böse D, Leineweber K, Konorza T, Zahn A, Brocker-Preuss M, Mann K et al. Release of TNF-a during stent implantation into saphenous vein aortocoronary bypass grafts and its relation to plaque extrusion and restenosis. Am J Physiol Heart Circ Physiol 2007;292:H2295-H2299.
96. Kleinbongard P, Heusch G, Schulz R. TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol Ther 2010;127:295-314.
97. Zhang C, Wu J, Xu X, Potter BJ, Gao X. Direct relationship between levels of TNF-alpha expression and endothelial dysfunction in reperfusion injury. Basic Res Cardiol 2010;105:453-464.
98. Bauer B, Simkhovich BZ, Kloner RA, Przyklenk K. Does preconditioning protect the coronary vasculature from subsequent ischemia/reperfusion injury? Circulation 1993; 88:659-672. (Pubitemid 23228067)
99. Richard V, Kaeffer N, Tron C, Thuillez C. Ischemic preconditioning protects against coronary endothelial dysfunction induced by ischemia and reperfusion. Circulation 1994;89:1254-1261. (Pubitemid 24076553)
100. Kaeffer N, Richard V, Francois A, Lallemand F, Henry JP, Thuillez C. Preconditioning prevents chronic reperfusion-induced coronary endothelial dysfunction in rats. Am J Physiol 1996;40:H842-H849.
101. Bouchard J-F, Lamontagne D. Mechanisms of protection afforded by preconditioning to endothelial function against ischemic injury. Am J Physiol 1996;271:H1801-H1806.
102. Bouchard J-F, Chouinard J, Lamontagne D. Role of kinins in the endothelial protective effect of ischaemic preconditioning. Br J Pharmacol 1998;123:413-420. (Pubitemid 28059709)
103. Thourani VH, Nakamura M, Duarte IG, Bufkin BL, Zhao Z-Q, Jordan JE et al. Ischemic preconditioning attenuates postischemic coronary artery endothelial dysfunction in a model of minimally invasive direct coronary artery bypass. J Thorac Cardiovasc Surg 1999;117:383-389. (Pubitemid 29068398)
104. Tofukuji M, Metais C, Li J, Hariawala MD, Franklin A, Vassileva C et al. Effects of ischemic preconditioning on myocardial perfusion, function, and microvascular regulation. Circulation 1998;98:II-197-II-205.
105. Loke KE, Woodman OL. Preconditioning improves myocardial function and reflow, but not vasodilator reactivity, after ischaemia and reperfusion in anaesthetized dogs. J Clin Exp Pharmacol Physiol 1998;25:552-558. (Pubitemid 28321620)
106. Gattullo D, Linden RJ, Losano G, Pagliario P, Westerhof N. Ischaemic preconditioning changes the pattern of coronary reative hyperaemia in the goat: role of adenosine and nitric oxide. Cardiovasc Res 1999;42:57-64. (Pubitemid 29167070)
107. Merkus D, Stepp DW, Jones DW, Nishikawa Y, Chilian WM. Adenosine preconditions against endothelin-induced constriction of coronary arterioles. Am J Physiol Heart Circ Physiol 2000;279:H2593-H2597. (Pubitemid 32005843)
108. Laude K, Favre J, Thuillez C, Richard V. NO produced by endothelial NO synthase is a mediator of delayed preconditioning-induced endothelial protection. Am J Physiol Heart Circ Physiol 2003;284:H2053-H2060. (Pubitemid 36622415)
109. Kim SJ, Zhang X, Xu X, Chen A, Gonzalez JB, Koul S et al. Evidence for enhanced eNOS function in coronary microvessels during the second window of protection. Am J Physiol Heart Circ Physiol 2007;292:H2152-H2158. (Pubitemid 47084594)
110. Shimizu M, Konstantinov IE, Kharbanda RK, Cheung MH, Redington AN. Effects of intermittent lower limb ischaemia on coronary blood flow and coronary resistance in pigs. Acta Physiol (Oxf) 2007;190:103-109. (Pubitemid 46776393)
111. Hoole SP, Heck PM, White PA, Khan SN, O'Sullivan M, Clarke SC et al. Remote ischemic preconditioning stimulus does not reduce microvascular resistance or improve myocardial blood flow in patients undergoing elective percutaneous coronary intervention. Angiology 2009;60:403-411.
112. Ma XJ, Zhang XH, Li CM, Luo M. Effect of postconditioning on coronary blood flow velocity and endothelial function in patients with acute myocardial infarction. Scand Cardiovasc J 2006;40:327-333. (Pubitemid 44803884)
113. Laskey WK, Yoon S, Calzada N, Ricciardi MJ. Concordant improvements in coronary flow reserve and ST-segment resolution during percutaneous coronary intervention for acute myocardial infarction: a benefit of postconditioning. Catheter Cardiovasc Interv 2008;72:212-220.
114. Garcia-Dorado D, Oliveras J, Gili J, Sanz E, Perez-Villa F, Barrabes J et al. Analysis of myocardial oedema by magnetic resonance imaging early after coronary artery occlusion with or without reperfusion. Cardiovasc Res 1993;27:1462-1469. (Pubitemid 23265067)
115. Abdel-Aty H, Cocker M, Meek C, Tyberg JV, Friedrich MG. Edema as a very early marker for acute myocardial ischemia: a cardiovascular magnetic resonance study. J Am Coll Cardiol 2009;53:1194-1201.
116. Garcia-Dorado D, Oliveras J. Myocardial edema: a preventable cause of reperfusion injury. Cardiovasc Res 1993;27:1555-1563. (Pubitemid 23297516)
117. Hori M, Gotoh K, Kitakaze M, Iwai K, Iwakura K, Sato H et al. Role of oxygen-derived free radicals in myocardial edema and ischemia in coronary microvascular embolization. Circulation 1991;84:828-840.
118. van den Berg BM, Vink H, Spaan JAE. The endothelial glycocalyx protects against myocardial edema. Circ Res 2003;92:592-594. (Pubitemid 36417691)
119. Chappell D, Hofmann-Kiefer K, Jacob M, Rehm M, Briegel J, Welsch U et al. TNF-alpha induced shedding of the endothelial glycocalyx is prevented by hydrocortisone and antithrombin. Basic Res Cardiol 2009;104:78-89.
120. Garcia-Dorado D, Théroux P, Munoz R, Alonso J, Elizaga J, Fernandez-Avilés F et al. Favorable effects of hyperosmotic reperfusion on myocardial edema and infarct size. Am J Physiol 1992;262:H17-H22.
121. Manciet LH, Poole DC, McDonagh PF, Copeland JG, Mathieu-Costello O. Microvascular compression during myocardial ischemia: mechanistic basis for no-reflow phenomenon. Am J Physiol 1994;266:H1541-H1550. (Pubitemid 24150786)
122. Sanz E, Dorado DG, Oliveras J, Barrabés JA, Gonzalez MA, Ruiz-Meana M et al. Dissociation between anti-infarct effect and anti-edema effect of ischemic preconditioning. Am J Physiol Heart Circ Physiol 1995;37:H233-H241.
123. Di Napoli P, Di Muzio M, Contegiacomo G, Tiloca P, Spoletini L, Di Crecchio A et al. Ischemic preconditioning of the myocardium: the role of changes in the permeability of the coronary microcirculation. Cardiologia 1997;42:59-67.
124. Breuckmann F, Nassenstein K, Bucher C, Konietzka I, Kaiser G, Konorza T et al. Systematic analysis of functional and structural changes after coronary microembolization: a cardiac magnetic resonance imaging study. JACC Imaging 2009;2:121-130.
125. Aletras AH, Tilak GS, Natanzon A, Hsu LY, Gonzalez FM, Hoyt RF Jr et al. Retrospective determination of the area at risk for reperfused acute myocardial infarction with T2-weighted cardiac magnetic resonance imaging: histopathological and displacement encoding with stimulated echoes (DENSE) functional validations. Circulation 2006;113:1865-1870. (Pubitemid 43739398)
126. Dall'armellina E, Karia N, Lindsay AC, Karamitsos TD, Ferreira V, Robson MD et al. Dynamic changes of edema and late gadolinium enhancement after acute myocardial infarction and their relationship to functional recovery and salvage index. Circ Cardiovasc Imaging 2011;4:228-236.
127. Wright J, Adriaenssens T, Dymarkowski S, Desmet W, Bogaert J. Quantification of myocardial area at risk with T2-weighted CMR: comparison with contrast-enhanced CMR and coronary angiography. JACC Cardiovasc Imaging 2009;2:825-831.
128. Wince WB, Kim RJ. Molecular imaging: T2-weighted CMR of the area at risk-a risky business? Nat Rev Cardiol 2010;7:547-549.
129. Kloner RA, Ganote CE, Jennings RB. The 'no-reflow' phenomenon after temporary coronary occlusion in the dog. J Clin Invest 1974;54:1496-1508.
130. Kloner RA. No-reflow phenomenon: maintaining vascular integrity. J Cardiovasc Pharmacol Ther 2011;16:244-250.
131. Jaffe R, Dick A, Strauss BH. Prevention and treatment of microvascular obstructionrelated myocardial injury and coronary no-reflow following percutaneous coronary intervention: a systematic approach. JACC Cardiovasc Interv 2010;3:695-704.
132. Niccoli G, Burzotta F, Galiuto L, Crea F. Myocardial no-reflow in humans. J Am Coll Cardiol 2009;54:281-292.
133. Bekkers SC, Yazdani SK, Virmani R, Waltenberger J. Microvascular obstruction: underlying pathophysiology and clinical diagnosis. J Am Coll Cardiol 2010;55: 1649-1660.
134. Posa A, Pavo N, Hemetsberger R, Csonka C, Csont T, Ferdinandy P et al. Protective effect of ischaemic preconditioning on ischaemia/reperfusion-induced microvascular obstruction determined by on-line measurements of coronary pressure and blood flow in pigs. Thromb Haemost 2010;103:450-460.
135. Zhao JL, Yang YJ, You SJ, Cui CJ, Gao RL. Different effects of postconditioning on myocardial no-reflow in the normal and hypercholesterolemic mini-swines. Microvasc Res 2007;73:137-142.
136. Hale SL, Mehra A, Leeka J, Kloner RA. Postconditioning fails to improve no reflow or alter infarct size in an open-chest rabbit model of myocardial ischemia-reperfusion. Am J Physiol Heart Circ Physiol 2008;294:H421-H425.
137. Reffelmann T, Kloner RA. Is microvascular protection by cariporide and ischemic preconditioning causally linked to myocardial salvage. Am J Physiol Heart Circ Physiol 2003;284:H1134-H1141. (Pubitemid 36348575)
138. Kunadian V, Zorkun C, Williams SP, Biller LH, Palmer AM, Ogando KJ et al. Intracoronary pharmacotherapy in the management of coronary microvascular dysfunction. J Thromb Thrombolysis 2008;26:234-242.
139. Heusch G. Adenosine and maximum coronary vasodilation in humans: myth and misconceptions in the assessment of coronary reserve. Basic Res Cardiol 2010;105:1-5.
140. Desmet W, Bogaert J, Dubois C, Sinnaeve P, Adriaenssens T, Pappas C et al. Highdose intracoronary adenosine for myocardial salvage in patients with acute ST-segment elevation myocardial infarction. Eur Heart J 2011;32:867-877.
141. Kleinbongard P, Böse D, Konorza T, Steinhilber F, Möhlenkamp S, Eggebrecht H et al. Acute vasomotor paralysis and potential downstream effects of paclitaxel from stents implanted for saphenous vein aorto-coronary bypass stenosis. Basic Res Cardiol 2011;106:681-689.