Reperfusion Microvascular Ischemia After Prolonged Coronary Occlusion: Implications And Treatment With Local Supersaturated Oxygen Delivery

References

• Jeremy RW, Links JM, Becker LC. Progressive failure of coronary flow during reperfusion of myocardial infarction: documentation of the no reflow phenomenon with positron emission tomography. J Am Coll Cardiol. 1990;16:695–704. doi:10.1016/0735-1097(90)90362-s
   PubMed Web of Science ®Google Scholar
• Wu KC, Zerhouni EA, Judd RM, et al. Prognostic significance of microvacular obstruction by magnetic resonance imaging in patients with acute myocardial infarction. Circulation. 1998;97:765–772. doi:10.1161/01.cir.97.8.765
   PubMed Web of Science ®Google Scholar
• Rochitte CE, Lima JAC, Bluemke DA, et al. The magnitude and time course of microvascular obstruction and tissue injury after acute myocardial infarction. Circulation. 1998;98:1006–1014. doi:10.1161/01.CIR.98.10.1006
   PubMed Web of Science ®Google Scholar
• O’Regan DP, Ariff B, Neuwirth C, Tan Y, Durighel G, Cook SA. Assessment of severe reperfusion injury with T2 cardiac MRI in patients with acute myocardial infarction. Heart. 2010;96:1885–1891. doi:10.1136/hrt.2010.200634
   PubMed Web of Science ®Google Scholar
• Ambrosio G, Weisman HF, Mannisi JA, Becker LC. Progressive impairment of regional myocardial perfusion after initial restoration of postischemic blood flow. Circulation. 1989;80:1846–1861. doi:10.1161/01.cir.80.6.1846
   PubMed Web of Science ®Google Scholar
• Pries AR, Habazettl H, Ambrosio G, et al. A review of methods for assessment of coronary microvascular disease in both clinical and experimental settings. Cardiovasc Res. 2008;80:165–174.
   PubMed Web of Science ®Google Scholar
• Swartz HM, Dunn JF. Measurements of oxygen in tissues: overview and perspectives on methods. Adv Exp Med Biol. 2003;530:1–12. doi:10.1007/978-1-4615-0075-9_1
   PubMed Web of Science ®Google Scholar
• Vikram DS, Zweier JL, Kuppusamy P. Methods for noninvasive imaging of tissue hypoxia. Antioxid Redox Signal. 2007;9:1745–1756. doi:10.1089/ars.2007.1717
   PubMed Web of Science ®Google Scholar
• Jain D, He Z-X. Direct imaging of myocardial ischemia: a potential new paradigm in nuclear cardiovascular imaging. J Nucl Card. 2008;15:617–630. doi:10.1016/j.nuclcard.2008.07.004
   PubMed Web of Science ®Google Scholar
• Handley MG, Medina RA, Nagel E, Blower PJ, Southworth R. PET imaging in cardiac hypoxia: opportunities and challenges. J Mol Cell Cardiol. 2011;51(5):640–650. doi:10.1016/j.yjmcc.2011.07.005
   PubMed Web of Science ®Google Scholar
• Bauer WR, Hiller K-H, Galuppo P, et al. Fast high-resolution magnetic resonance imaging demonstrates fractality of myocardial perfusion in microscopic dimensions. Circ Res. 2001;88:340–346. doi:10.1161/01.res.88.3.340
   PubMed Web of Science ®Google Scholar
• Zuurbier CJ, van Iterson M, Ince C. Functional heterogeneity of oxygen supply-consumption ratio in the heart. Cardiovasc Res. 1999;44:488–497. doi:10.1016/s0008-6363(99)00231-x
   PubMed Web of Science ®Google Scholar
• Balaban RS, Arai A. Function, metabolic, and flow heterogeneity of the heart. The View Is Getting Better. Circ Res. 2001;88:265–267.
   PubMed Web of Science ®Google Scholar
• Pries AR, Secomb TW. Origins of heterogeneity in tissue perfusion and metabolism. Cardiovasc Res. 2009;81:328–335. doi:10.1093/cvr/cvn318
   PubMed Web of Science ®Google Scholar
• Ghaleh B, Shen YT, Vatner SF. Spatial heterogeneity of myocardial blood flow presages salvage versus necrosis with coronary artery reperfusion in conscious baboons. Circulation. 1996;94:2210–2215. doi:10.1161/01.cir.94.9.2210
   PubMedGoogle Scholar
• Steenbergen C, Deleeuw G, Barlow C, Chance B, Williamson JR. Heterogeneity of the hypoxic state in perfused rat heart. Circ Res. 1977;41:606–615. doi:10.1161/01.res.41.5.606
   PubMed Web of Science ®Google Scholar
• Ince C, Vink H, Wieringa PA, Giezeman M, Spaan JA. Heterogeneous NADH fluorescence during post-anoxic hyperemia in saline perfused heart. Adv Exp Med Biol. 1990;277:477–482. doi:10.1007/978-1-4684-8181-5_53
   PubMedGoogle Scholar
• Ince C, Ashruf JF, Avontuur JA, Wieringa PA, Spaan JA, Bruining HA. Heterogeneity of the hypoxic state in rat heart is determined at the capillary level. Am J Physiol. 1993;264:H294–H301. doi:10.1152/ajpheart.1993.264.2.H294
   PubMedGoogle Scholar
• Vetterlein F, Prange M, Lubrich D, Pedina J, Neckel M, Schmidt G. Capillary perfusion pattern and microvascular geometry in heterogeneous hypoxic areas of hypoperfused rat myocardium. Am J Physiol. 1995;268:H2183–H2194. doi:10.1152/ajpheart.1995.268.6.H2183
   PubMedGoogle Scholar
• Groner W, Winkelman JW, Harris AG, et al. Orthogonal polarization spectral imaging: a new method for study of the microcirculation. Nat Med. 1999;5:1209–1212. doi:10.1038/13529
   PubMed Web of Science ®Google Scholar
• De Backer D, Ospina-Tascon G, Salgado D, Favory R, Creteur J, Vincent JL. Monitoring the microcirculation in the critically ill patient: current methods and future approaches. Intensive Care Med. 2010;36:1813–1825. doi:10.1007/s00134-010-2005-3
   PubMed Web of Science ®Google Scholar
• Sakr Y, Dubois M-J, De Backer D, Creteur J, Vincent J-L. Persistent microcirculatory alterations are associated with organ failure in patients with septic shock. Crit Care Med. 2004;32:1825–1831. doi:10.1097/01.ccm.0000138558.16257.3f
   PubMed Web of Science ®Google Scholar
• Ellis CG, Bateman RM, Sharpe MD, Sibbald WJ, Gill R. Effect of maldistribution of microvascular blood flow on capillary O2 extraction in sepsis. Am J Physiol Heart Circ Physiol. 2002;2002(282):H156–H164. doi:10.1152/ajpheart.2002.282.1.H156
   Google Scholar
• De Backer D, Creteur J, Dubois MJ, Sakr Y, Vincent JL. Microvascular alterations in patients with acute severe heart failure and cardiogenic shock. Am Heart J. 2004;147:91–99. doi:10.1016/j.ahj.2003.07.006
   PubMed Web of Science ®Google Scholar
• De Backer D, Dubois MJ, Schmartz D, et al. Microcirculatory alterations in cardiac surgery: effects of cardiopulmonary bypass and anesthesia. Ann Thorac Surg. 2009;88:1396–1403. doi:10.1016/j.athoracsur.2009.07.002
   PubMed Web of Science ®Google Scholar
• Camilleri JP, Nlom MO, Michel JB, Barres D, Mignot J. Capillary perfusion patterns in reperfused ischemic subendocardial myocardium: experimental study using fluorescent dextran. Exp Mol Pathol. 1983;39:89–99. doi:10.1016/0014-4800(83)90043-6
   PubMed Web of Science ®Google Scholar
• Downey HF, Bashour FA, Jishi B, Parker PE. Arteriovenous shunts in dilated or reperfused canine coronary vasculature. Microvasc Res. 1979;17:22–26. doi:10.1016/0026-2862(79)90004-9
   PubMed Web of Science ®Google Scholar
• Weis S, Shintani S, Weber A, et al. Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J Clin Invest. 2004;113:885–894. doi:10.1172/JCI20702
   PubMed Web of Science ®Google Scholar
• Kay M, Swift L, Martell B, Aruntunyan A, Sarvazyan N. Locations of ectopic beats coincide with spatial gradients of NADH in a regional model of low-flow reperfusion. Am J Physiol Heart Circ Physiol. 2008;294:H2400–H2405. doi:10.1152/ajpheart.01158.2007
   PubMed Web of Science ®Google Scholar
• Wang B, Ansari R, Sun Y, Postlethwaite AE, Weber KT, Kiani MF. The scar neovasculature after myocardial infarction in rats. Am J Physiol Heart Circ Physiol. 2005;289:H108–H113. doi:10.1152/ajpheart.00001.2005
   PubMed Web of Science ®Google Scholar
• Wang B, Scott RC, Pattillo CB, Prabhakarpandian B, Sundaram S, Kiani MF. Microvascular transport model predicts oxygenation changes in the infarcted heart after treatment. Am J Physiol Heart Circ Physiol. 2007;293:H3732–H3739. doi:10.1152/ajpheart.00735.2007
   PubMed Web of Science ®Google Scholar
• Al-Obaidi MK, Etherington PJ, Barron DJ, Winlove CP, Pepper JR. Myocardial tissue oxygen supply and utilization during coronary artery bypass surgery: evidence of microvascular no-reflow. Clin Sci. 2000;98:321–328. doi:10.1042/cs0980321
   Web of Science ®Google Scholar
• Pathi VL, McPhaden AR, Morrison J, et al. The effects of cardioplegic arrest and reperfusion on the microvasculature of the heart. Europ J Cardio-Thor Surg. 1997;11:350–357. doi:10.1016/S1010-7940(96)01037-8
   PubMed Web of Science ®Google Scholar
• Lipowski HH. Microvascular rheology and hemodynamics. Microcirculation. 2005;12:5–15. doi:10.1080/10739680590894966
   PubMed Web of Science ®Google Scholar
• Boerma EC, Ince C. The role of vasoactive agents in the resuscitation of microvascular perfusion and tissue oxygenation in critically ill patients. Intensive Card Med. 2010;36:2004–2018. doi:10.1007/s00134-010-1970-x
   PubMed Web of Science ®Google Scholar
• Eliasen P, Amtorp O. Oxygen transport to the canine left ventricle distal to a flow-limiting coronary artery stenosis. Int J Microcirc Clin Exp. 1985;4:329–341.
   PubMedGoogle Scholar
• Barker MC, Golub AS, Pittman RN. Erythrocyte-associated transients in capillary PO2: an isovolemic hemodilution study in rat spinotrapezius muscle. Am J Physiol Heart Circ Physiol. 2007;292:H2540–H2549. doi:10.1152/ajpheart.00915.2006
   PubMed Web of Science ®Google Scholar
• Goldman D, Bateman RM, Ellis CG. Effect of sepsis on skeletal muscle oxygen consumption and tissue oxygenation: interpreting capillary oxygen transport data using a mathematical model. Am J Physiol Heart Circ Physiol. 2004;287:H2535–H2544. doi:10.1152/ajpheart.00889.2003
   PubMed Web of Science ®Google Scholar
• Connett RJ, Honig CR, Gayeski TE, Brooks GA. Defining hypoxia: a systems view of VO2, glycolysis, energetics, and intracellular pO2. J Appl Physiol. 1990;68:833–842. doi:10.1152/jappl.1990.68.3.833
   PubMed Web of Science ®Google Scholar
• Sezer M, van Royen N, Umman B, et al. Coronary microvascular injury in reperfused acute myocardial infarction: a view from an integrative perspective. J Am Heart Assoc. 2018;7(21):e009949. doi:10.1161/JAHA.118.008528
   PubMed Web of Science ®Google Scholar
• Kloner RA, Dai W, Hale SL. No-reflow phenomenon. A new target for therapy of acute myocardial infarction independent of myocardial infarct size. J Cardiovasc Pharmacol Ther. 2018;23(3):273–276.
   PubMed Web of Science ®Google Scholar
• Hori M, Inoue M, Kitakaze M, et al. Role of adenosine in hyperemic response of coronary blood flow in microcirculation. Am J Physiol. 1986;250:H509–H518. doi:10.1152/ajpheart.1986.250.3.H509
   PubMedGoogle Scholar
• Kassab GS, Rider CA, Tang NJ, Fung YC. Morphometry of pig coronary arterial trees. Am J Physiol. 1993;265:H350–H365. doi:10.1152/ajpheart.1993.265.1.H350
   PubMed Web of Science ®Google Scholar
• Wang X, Peter K. Molecular imaging of atherothrombotic diseases. Seeing Is Believing. Arterioscler Thromb Vasc Biol. 2017;37:1029–1040. doi:10.1161/ATVBAHA.116.306483
   PubMed Web of Science ®Google Scholar
• Ziegler M, Alt K, Paterson BM, et al. Highly sensitive detection of minimal cardiac ischemia using positron emission tomography imaging of activated platelets. Sci Rep. 2016;6:38161. doi:10.1038/srep38161
   PubMed Web of Science ®Google Scholar
• Liu S, Liu W, Ding W, Miyake M, GA R, Liu KJ. Electron paramagnetic resonance-guided normobaric hyperoxia treatment protects the brain by maintaining penumbral oxygenation in a rat model of transient focal cerebral ischemia. J Cereb Blood Flow Metab. 2006;26:1274–1284. doi:10.1038/sj.jcbfm.9600277
   PubMed Web of Science ®Google Scholar
• Quintero M, Colombo SL, Godfrey A, Moncada S. Mitochondria as signaling organelles in the vascular endothelium. Proc Natl Acad Sci USA. 2006;103:5379–5384. doi:10.1073/pnas.0601026103
   PubMed Web of Science ®Google Scholar
• Ten VS, Pinsky DJ. Endothelial response to hypoxia: physiologic adaptation and pathologic dysfunction. Curr Opin Crit Care. 2002;8:242–250.
   PubMedGoogle Scholar
• Michiels C. Physiological and pathological responses to hypoxia. Am J Pathol. 2004;164:1875–1882. doi:10.1016/S0002-9440(10)63747-9
   PubMed Web of Science ®Google Scholar
• Pober JS. Physiology and pathobiology of microvascular endothelium. In: Tuma RE, Duran WN, Ley K, editors. Handbook of Physiology: Microcirculation. 2nd ed. San Diego: Elsevier; 2008:37–55. ISBN: 978-0-12-374530-9
   Google Scholar
• Pober JS. Physiology and Pathobiology of Microvascular Endothelium. Compr Physiol. 2011; Supplement 9:37–55. Handbook of Physiology, The Cardiovascular System, Microcirculation. First published in print 2008. doi: 10.1002/cphy.cp020402.
   Google Scholar
• Aird WC. Spatial and temporal dynamics of the endothelium. J Thromb Haemostasis. 2005;3:1392–1406. doi:10.1111/j.1538-7836.2005.01328.x
   PubMed Web of Science ®Google Scholar
• Matsushita H, Morishita R, Nata T, et al. Hypoxia-induced endothelial apoptosis through nuclear factor-kB (NF-kB)-mediated bcl-2 suppression. In vivo evidence of the importance of NF-kB in endothelial cell regulation. Circ Res. 2000;86:974–981. doi:10.1161/01.res.86.9.974
   PubMed Web of Science ®Google Scholar
• Walford GA, Moussignac R-L, Scribner AW, Loscalzo J, Leopold JA. Hypoxia potentiates nitric oxide-mediated apoptosis in endothelial cells via peroxynitrite-induced activation of mitochondria-dependent and -independent pathways. JBC. 2004;279:4425–4432. doi:10.1074/jbc.M310582200
   PubMed Web of Science ®Google Scholar
• Ohta T, Eguchi R, Suzuki A, Miyakaze S, Ayuzawa R, Kaji K. Hypoxia-induced apoptosis and tube breakdown are regulated by p38 MAPK but not by caspase cascade in an in vitro capillary model composed of human endothelial cells. J Cell Physiol. 2007;211:673. doi:10.1002/jcp.20975
   PubMed Web of Science ®Google Scholar
• Manalo DJ, Rowan A, Lavoie T, et al. Transcriptional regulation of vascular endothelial responses to hypoxia by HIF-1. Blood. 2005;105:659–669. doi:10.1182/blood-2004-07-2958
   PubMed Web of Science ®Google Scholar
• Winning S, Splettstoesser F, Fandrey J, Frede S. Acute hypoxia induces HIF-independent monocyte adhesion to endothelial cells through increased intercellular adhesion molecule-1 expression: the role of hypoxic inhibition of prolyl hydroxylase activity for the induction of NF-kappa B. J Immunol. 2010;185:1786–1793. doi:10.4049/jimmunol.0903244
   PubMed Web of Science ®Google Scholar
• Tian F, Zhou AX, Smits AM, et al. Endothelial cells are activated during hypoxia via endoglin/ALK-1/SMAD1/5 signaling in vivo and in vitro. Biochem Biophys Res Commun. 2010;392:283–288. doi:10.1016/j.bbrc.2009.12.170
   PubMed Web of Science ®Google Scholar
• Rao RM, Yang L, Garcia-Cardena G, Luscinskas FW. Endothelial-dependent mechanisms of leukocyte recruitment to the vascular wall. Circ Res. 2007;101:234–247. doi:10.1161/CIRCRESAHA.107.151860b
   PubMed Web of Science ®Google Scholar
• He P. Leucocyte/endothelium interactions and microvessel permeability: coupled or uncoupled? Cardiovasc Res. 2010;87:281–290. doi:10.1093/cvr/cvq140
   PubMed Web of Science ®Google Scholar
• Bartels K, Grenz A, and Elzschig HK. Hypoxia and inflammation are two sides of the same coin. PNAS. 2013;110(46):18351–18352. doi:10.1073/pnas.1318345110
   PubMed Web of Science ®Google Scholar
• Eltzchig HK, Carmeliet P. Hypoxia and inflammation. New Engl J Med. 2011;364:656–665. doi:10.1056/NEJMra0910283
   PubMedGoogle Scholar
• Aversa CR, Oparil S, Caro J, et al. Hypoxia stimulates human proendothelin-1 promoter activity in transgenic mice. Am J Physiol. 1997;273:L848–L855. doi:10.1152/ajplung.1997.273.4.L848
   PubMedGoogle Scholar
• Parthasarathi K, Lipowski HH. Capillary recruitment in response to tissue hypoxia and its dependence on red cell deformability. Amer J Physiol Heart Circ Physiol. 1999;46:H2145–H2157. doi:10.1152/ajpheart.1999.277.6.H2145
   Google Scholar
• Ritter LS, McDonagh PF. Low-flow reperfusion after myocardial ischemia enhances leukocyte accumulation in coronary microcirculation. Am J Physiol. 1997;273:H1154–H1165.
   PubMedGoogle Scholar
• Kubes P. The role of shear forces in ischemia/reperfusion-induced neutrophil rolling and adhesion. J Leukoc Biol. 1997;62:458–464. doi:10.1002/jlb.62.2.268
   PubMed Web of Science ®Google Scholar
• Eppihimer MJ, Lipowski HH. Leukocyte sequestration in the microvasculature in normal and low flow states. Am J Physiol. 1994;267:H1122–H1134. doi:10.1152/ajpheart.1994.267.3.H1122
   PubMedGoogle Scholar
• Sriramarao P, Languino LR, Altieri DC. Fibrinogen mediates leukocyte-endothelium bridging in vivo at low shear forces. Blood. 1996;88:3416–3423.
   PubMed Web of Science ®Google Scholar
• Hahn C, Schwartz MA. Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol. 2009;10:53–62. doi:10.1038/nrm2596
   PubMed Web of Science ®Google Scholar
• Bassiouny HS, Song RH, Kocharyan H, Kins E, Glagov S. Low flow enhances platelet activation after acute experimental arterial injury. J Vasc Surg. 1997;27:910–918. doi:10.1016/S0741-5214(98)70272-1
   Web of Science ®Google Scholar
• Dongaonkar RM, Stewart RH, Geissler HJ, Laine GA. Myocardial microvascular permeability, interstitial oedema, and compromised cardiac function. Cardiovasc Res. 2010;87:331–339. doi:10.1093/cvr/cvq145
   PubMed Web of Science ®Google Scholar
• Tang Y, Nyengaard JR, Andersen JB, Baandrup U, Gundersen HJG. The application of stereological methods for estimating structural parameters in the human heart. Anat Rec. 2009;292:1630–1647. doi:10.1002/ar.20952
   Google Scholar
• Pries AR, Neuhaus D, Gaehtgens P. Blood viscosity in tube flow: dependence on diameter and hematocrit. Am J Physiol. 1992;263:H1770–H1778. doi:10.1152/ajpheart.1992.263.6.H1770
   PubMed Web of Science ®Google Scholar
• Vince RV, Chrismas B, Midgley AW, McNaughton LR, Madden LA. Hypoxia mediated release of endothelial microparticles and increased association of S100A12 with circulating neutrophils. Oxid Med Cell Longev. 2009;2:2–6.
   PubMed Web of Science ®Google Scholar
• Boerma EC, Ince C. The role of vasoactive agents in the resuscitation of microvacular perfusion and tissue oxygenation in critically ill patients. Intensive Care Med. 2010;36:2004–2018. doi:10.1007/s00134-010-1970-x
   PubMed Web of Science ®Google Scholar
• Ogawa S, Shreeniwas R, Brett J, Clauss M, Furie M, Stern DM. The effect of hypoxia on capillary endothelial cell function: modulation of barrier and coagulant function. Br J Haematol. 1990;75(4):517–524. doi:10.1111/j.1365-2141.1990.tb07792.x
   PubMed Web of Science ®Google Scholar
• Gupta N, Zhao -Y-Y, Evans CE. The stimulation of thrombosis by hypoxia. Thromb Res. 2019;181:77–83. doi:10.1016/j.thromres.2019.07.013
   PubMed Web of Science ®Google Scholar
• Gertler JP, Perry L, L’Italien G, et al. Ambient oxygen tension modulates endothelial fibrinolysis. J Vasc Surg. 1993;18(6):939–946.
   PubMed Web of Science ®Google Scholar
• Ponicke K, Sternitsky R, Mest HJ. Stimulation of aggregation and thromboxane A2 formation of human platelets by hypoxia. Prostaglandins Leukot Med. 1987;29:49–59.
   PubMedGoogle Scholar
• Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K, Dalkara T. Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med. 2009;15:1031–1037. doi:10.1038/nm.2022
   PubMed Web of Science ®Google Scholar
• Schulze C, Firth JA. Junctions between pericytes and the endothelium in rat myocardial capillaries: a morphometric and immunogold study. Cell Tissue Res. 1993;271:145–154. doi:10.1007/bf00297552
   PubMed Web of Science ®Google Scholar
• Glyn MC, Lawrenson JG, Ward BJ. Change in endothelial cell shape in response to ischaemia in the cardiac and retinal capillary beds. J Anat. 2002;200:526–534. doi:10.1046/j.1469-7580.2002.00047_11.x
   Google Scholar
• Chenghai S, Jain RK, Munn LL. Non-uniform plasma leakage affects local hematocrit and blood flow: implications for inflammation and tumor perfusion. Ann Biomed Eng. 2007;35:2121–2129. doi:10.1007/s10439-007-9377-8
   PubMed Web of Science ®Google Scholar
• Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol. 2000;88:1474–1480. doi:10.1152/jappl.2000.88.4.1474
   PubMed Web of Science ®Google Scholar
• Battino R, ed, Oxygen Data Series, Vol 7: Oxygen and Ozone. New York, NY: Pergamon Press; 1981:1–40.
   Google Scholar
• Hofmann R, James SK, Jernberg T, et al. Oxygen therapy in suspected acute myocardial infarction. N Engl J Med. 2017;377:1240–1249. doi:10.1056/NEJMoa1706222
   PubMed Web of Science ®Google Scholar
• Khoshnood A, Carlsson M, Akbarzadeh M, et al. Effect of oxygen therapy on myocardial salvage in ST elevation myocardial infarction: the randomized SOOCER trial. Eur J Emerg Med. 2018;25(2):78–84. doi:10.1097/MEJ.0000000000000431
   PubMed Web of Science ®Google Scholar
• Sepehrvand N, James SK, Stub D, Khosnood A, Ezekowitz JA, Hofmann R. Effect of supplemental oxygen therapy in patients with suspected acute myocardial infarction: a meta-analysis of randomized clinical trials. Heart. 2018;104(20):1691–1698. doi:10.1136/heartjnl-2018-313089
   PubMed Web of Science ®Google Scholar
• Van Meter KW. A systematic review of the application of hyperbaric oxygen in the treatment of severe anemia: an evidence-based approach. Undersea Hyperb Med. 2005;32:61–83.
   PubMed Web of Science ®Google Scholar
• Duling BR. Microvascular responses to alterations in oxygen tension. Circ Res. 1972;31:481–489. doi:10.1161/01.res.31.4.481
   PubMed Web of Science ®Google Scholar
• Piantadosi CA. Pulmonary gas exchange, oxygen transport, and tissue oxygenation. In: Neuman TS, Thom SR, editors. Physiology and Medicine of Hyperbaric Oxygen Therapy. Philadelphia: Saunders; 2008:133–158.
   Google Scholar
• Cason BA, Wisneski JA, Neese RA, et al. Effects of high arterial oxygen tension on function, blood flow distribution, and metabolism in ischemic myocardium. Circulation. 1992;85:828–838. doi:10.1161/01.cir.85.2.828
   PubMed Web of Science ®Google Scholar
• Ribeiro LGT, Louie EK, Davis MA, Maroko PR. Augmentation of collateral blood flow to the ischemia myocardium by oxygen inhalation following experimental coronary artery occlusion. Cardiovasc Res. 1979;13:160–166. doi:10.1093/cvr/13.3.160
   PubMed Web of Science ®Google Scholar
• Spears JR, Wang B, Wu X, et al. Aqueous oxygen: a highly O2-supersaturated infusate for regional correction of hypoxemia and production of hyperoxemia. Circulation. 1997;96:4385–4391. doi:10.1161/01.cir.96.12.4385
   PubMed Web of Science ®Google Scholar
• Brereton GJ, Crilly RJ, Spears JR. Nucleation in small capillary tubes. Chem Phys. 1998;230:253–265. doi:10.1016/S0301-0104(98)00052-4
   Web of Science ®Google Scholar
• Dixon SR, O’Neill WW, Bartorelli AL, et al. Early recovery of infarct zone function with intracoronary hyperoxemia reperfusion after primary angioplasty for acute myocardial infarction. JACC. 2002;39:387–392. doi:10.1016/s0735-1097(01)01771-5
   Google Scholar
• Propel AS, Gross JF. Analysis of oxygen diffusion from arteriolar networks. Amer J Physiol. 1979;237:H681–H689. doi:10.1152/ajpheart.1979.237.6.H681
   PubMedGoogle Scholar
• Sharan M, Singh MP, Singh B. An analytical model for oxygen transport in tissue capillaries in a hyperbaric environment with first order metabolic consumption. Math Comput Modelling. 1995;22:99–111. doi:10.1016/0895-7177(95)00171-W
   Google Scholar
• Reffelmann T, Kloner RA. The “no-reflow” phenomenon: basic science and clinical correlates. Heart. 2002;87:162–168. doi:10.1136/heart.87.2.162
   PubMed Web of Science ®Google Scholar
• Prasad A, Stone GW, Holmes DR, Gersh B. Reperfusion injury, microvascular dysfunction, and cardioprotection. The “dark side” of reperfusion. Circulation. 2009;120:2105–2112. doi:10.1161/CIRCULATIONAHA.108.814640
   PubMed Web of Science ®Google Scholar
• Rodrigues SF, Granger DN. Role of blood cells in ischemia-reperfusion induced endothelial barrier failure. Cardiovasc Res. 2010;87:291–299. doi:10.1093/cvr/cvq090
   PubMed Web of Science ®Google Scholar
• Bekkers SCAM, Yazdani SK, Virmani R, Waltenberger J. Microvascular obstruction: underlying pathophysiology and clinical diagnosis. J Am Coll Cardiol. 2010;55:1649–1660. doi:10.1016/j.jacc.2009.12.037
   PubMed Web of Science ®Google Scholar
• Thurston JGB, Greenwood TW, Bending MR, Connor H, Curwen MP. A controlled investigation into the effects of hyperbaric oxygen on mortality following acute myocardial infarction. Q J Med. 1973;42:751–770.
   PubMedGoogle Scholar
• Stavitsky Y, Shandling AH, Ellestadt MH, et al. Hyperbaric oxygen and thrombolysis in myocardial infarction: the “HOT MI” randomized mulitcenter study. Cardiology. 1998;90:131–136. doi:10.1159/000006832
   PubMed Web of Science ®Google Scholar
• Dekleva M, Neskovic A, Vlahovic A, Putnikovic B, Beleslin B, Ostojic M. Adjunctive effect of hyperbaric oxygen treatment after thrombolysis on left ventricular function in patients with acute myocardial infarction. Am Heart J. 2004;148:E14. doi:10.1016/j.ahj.2004.05.032
   PubMed Web of Science ®Google Scholar
• Sharifi M, Fares W, Abdel-Karim I, Koch JM, Sopko J, Adler D. Usefulness of hyperbaric oxygen therapy to inhibit restenosis after percutaneous coronary intervention for acute myocardial infarction or unstable angina pectoris. Am J Cardiol. 2004;93:1533–1535. doi:10.1016/j.amjcard.2004.03.009
   PubMed Web of Science ®Google Scholar
• Bennett MH, Lehm JP, Jepson N. Hyperbaric oxygen therapy for acute coronary syndrome. Cochrane Database Syst Rev. 2015;(7): CD004818.
   Google Scholar
• Ambiru S, Furuyama N, Aono M, Otsuka H, Suzuki T, Miyazaki M. Analysis of risk factors associated with complications of hyperbaric oxygen therapy. J Crit Care. 2008;23:295–300. doi:10.1016/j.jcrc.2007.08.002
   PubMed Web of Science ®Google Scholar
• Perrins DJD, Cantab MB. Influence of hyperbaric oxygen on the survival of split skin grafts. Lancet. 1967;II:868–871. doi:10.1016/S0140-6736(67)91428-6
   Google Scholar
• Bouachour G, Cronier P, Gouello JP, Toulemonde JL, Talha A, Alquier P. Hyperbaric oxygen therapy in the management of crush injuries: a randomized double-blinded placebo-controlled clinical trial. J Trauma. 1996;41:333–339. doi:10.1097/00005373-199608000-00023
   PubMedGoogle Scholar
• Weaver LK, Hopkins RO, Chan KJ, et al. Hyperbaric oxygen for acute carbon monoxide poisoning. N Engl J Med. 2002;347:1057–1067. doi:10.1056/NEJMoa013121
   PubMed Web of Science ®Google Scholar
• Buras JA, Garcia-Covarrubias L. Ischemia-reperfusion injury: hyperbaric oxygen and basic studies. In: Neuman TS, Thom SR, editors. Physiology and Medicine of Hyperbaric Oxygen Therapy. Philadelphia: Saunders Elsevier; 2008:160–184.
   Google Scholar
• Van Meter K, Sheps S, Kriedt F, et al. Hyperbaric oxygen improves rate of return of spontaneous circulation after prolonged normothermic porcine cardiopulmonary arrest. Resuscitation. 2008;78:200–214. doi:10.1016/j.resuscitation.2008.02.026
   PubMed Web of Science ®Google Scholar
• Oter S, Radermacher S, Matejovic M. Can (hyperbaric) oxygen turn off the motor of multiorgan dysfunction? Intensive Care Med. 2006;32:1694–1696.
   PubMed Web of Science ®Google Scholar
• Spears JR, Henney C, Prcevski P, et al. Reperfusion microvascular ischemia attenuated with aqueous oxygen infusion in a porcine coronary occlusion model. Circulation. 1999;102(Suppl. I):I–512. abstract, presented by Spears JR at the 72nd Scientific Sessions of the AHA, November 1999.
   Google Scholar
• Spears JR, Prcevski P, Xu R, et al. Aqueous oxygen attenuation of reperfusion microvascular ischemia in a canine model of myocardial infarction. Asaio J. 2003;49:716–720. doi:10.1097/01.mat.0000094665.72503.3c
   PubMed Web of Science ®Google Scholar
• Spears JR, Henney C, Prcevski P, et al. Aqueous oxygen hyperbaric reperfusion in a porcine model of myocardial infarction. J Invas Cardiol. 2002;14:160–166.
   PubMedGoogle Scholar
• Johnson LL, Schofield L, Bouchard M, et al. Hyperbaric oxygen solution infused into the anterior interventricular vein at reperfusion reduces infarct size in swine. Am J Physiol Heart Circ Physiol. 2004;287:H2234–H2240. doi:10.1152/ajpheart.00333.2003
   PubMed Web of Science ®Google Scholar
• Glazier JJ. Attenuation of reperfusion microvascular ischemia by aqueous oxygen: experimental and clinical observations. Am Heart J. 2005;149:580–584. doi:10.1016/j.ahj.2004.12.009
   PubMed Web of Science ®Google Scholar
• Bartorelli AL. Hyperoxemic perfusion for treatment of reperfusion microvascular ischemia in patients with myocardial infarction. Am J Cardiovasc Drugs. 2003;3:253–263. doi:10.2165/00129784-200303040-00004
   PubMedGoogle Scholar
• Spears JR, Prcevski P, Jiang A, Brereton GJ, Vander Heide R. Intracoronary aqueous oxygen perfusion, performed 24 hrs after the onset of postinfarction reperfusion, experimentally reduces infarct size and improves left ventricular function. Int J Cardiol. 2006;113:371–5.
   PubMed Web of Science ®Google Scholar
• Dixon SR, Bartorelli AL, Marcovitz PA, et al. Initial experience with hyperoxemic reperfusion after primary angioplasty for acute myocardial infarction: results of a pilot study utilizing intracoronary aqueous oxygen therapy. J Am Coll Cardiol. 2002;39:387–392. doi:10.1016/s0735-1097(01)01771-5
   PubMed Web of Science ®Google Scholar
• Trabbatoni D, Bartorelli AL, Fabbiocchi F, et al. Hyperoxemic perfusion of the left anterior descending coronary artery after primary angioplasty in anterior ST-elevation myocardial infarction. Catheter Cardiovasc Interv. 2006;67:859–865. doi:10.1002/ccd.20704
   PubMed Web of Science ®Google Scholar
• O’Neill WW, Martin JL, Dixon SR, et al.; AMIHOT Investigators. Acute myocardial infarction with hyperoxemic therapy (AMIHOT): a prospective, randomized trial of intracoronary hyperoxemic reperfusion after percutaneous coronary intervention. J Am Coll Cardiol. 2007;50:397–405. doi:10.1016/j.jacc.2007.01.099
   PubMed Web of Science ®Google Scholar
• Stone GW, Martin JL, de Boer M-J, et al., for the AMIHOT-II Trial Investigators. Effect of supersaturated oxygen delivery on infarct size after percutaneous coronary intervention in acute myocardial infarction. Circulation. 2009;2:366–375.
   PubMed Web of Science ®Google Scholar
• David SW, Khan ZA, Patel NC, et al. Evaluation of intracoronary hyperoxemic oxygen therapy in acute anterior myocardial infarction: the IC-HOT study. Catheter Cardiovasc Interv. 2019;93(5):882–890.
   PubMed Web of Science ®Google Scholar
• Stone GW. Symposium Chairman, SuperSaturated Oxygen in STEMI to Reduce Infarct Size: A New FDA-Approved Therapy. Oral presentation: SSO2 Therapy: Clinical Evidence and Outcomes. TCT Conference, San Francisco, CA, September 26, 2019
   Google Scholar
• Ali MH, Schlidt SA, Chandel NS, Hynes KL, Schumacker PT, Gewertz BL. Endothelial permeability and IL-9 production during hypoxia: role of ROS in signal transduction. Am J Physiol. 1999;277:L1057–L1065. doi:10.1152/ajplung.1999.277.5.L1057
   PubMed Web of Science ®Google Scholar
• Schmitz K, Jennewein M, Pohlemann T, Seekamp A, Oberringer M. Reoxygenation attenuates the adhesion of neutrophils to microvascular endothelial cells. Angiology. 2011;62:155–162. doi:10.1177/0003319710375943
   PubMed Web of Science ®Google Scholar
• Hinshaw DB, Armstrong BC, Beals TF, Hyslop PA. A cellular model of endothelial cell ischemia. J Surg Res. 1988;44:527–537. doi:10.1016/0022-4804(88)90158-8
   PubMed Web of Science ®Google Scholar
• Chen C-A, Wang T-Y, Varadharaj S, et al. S-gluthionylation uncouples eNOS and regulates its cellular and vascular function. Nature. 2010;468:1115–1118. doi:10.1038/nature09599
   PubMed Web of Science ®Google Scholar
• Fish JE, Yan MS, Matouk CC, et al. Hypoxic repression of endothelial nitric-oxide synthase transcription is coupled with eviction of promoter histones. J Biol Chem. 2010;285:810–826. doi:10.1074/jbc.M109.067868
   PubMed Web of Science ®Google Scholar
• Huang B, Chen SC, Wang DL. Shear flow increases S-nitrosylation of proteins in endothelial cells. Cardiovasc Res. 2009;83:536–546. doi:10.1093/cvr/cvp154
   PubMed Web of Science ®Google Scholar
• Stamenkovic A, Pierce GN, Ravandi A. Review: Many avenues to cardiac cell death. Phospholipid oxidation products in ferroptotic myocardial cell death. Am J Physiol Heart Circ Physiol. 2019;317:H156–H163. doi:10.1152/ajpheart.00076.2019
   PubMed Web of Science ®Google Scholar
• Tang D, Kang R, Vanden Berghe T, Vandenabeele P, Kroemer G. The molecular machinery of regulated cell death. Cell Research. 2019;29:347–364. doi:10.1038/s41422-019-0164-5
   PubMed Web of Science ®Google Scholar
• Clarke SJ, Khaliulin I, Das M, Parker JE, Heesom KJ, Halestrap AP. Inhibition of mitochondrial permeability transition pore opening by ischemic preconditioning is probably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation. Circ Res. 2008;102:1082–1090. doi:10.1161/CIRCRESAHA.107.167072
   PubMed Web of Science ®Google Scholar
• Scarabelli T, Stephanou A, Rayment N, et al. Apoptosis of endothelial cells precedes myocyte cell apoptosis in ischemia/reperfusion injury. Circulation. 2001;104:253. doi:10.1161/01.CIR.104.3.253
   PubMed Web of Science ®Google Scholar
• Pozzi S, Malferrari G, Biunno I, Samaja M. Low-flow ischemia and hypoxia stimulate apoptosis in perfused hearts independently of reperfusion. Cell Physiol Biochem. 2002;12:39–46. doi:10.1159/000047825
   PubMedGoogle Scholar
• Bragadeesh T, Jayaweera AR, Pascotto M, et al. Post-ischemic myocardial dysfunction (stunning) results from myofibrillar oedema. Heart. 2008;94:166–171. doi:10.1136/hrt.2006.102434
   PubMed Web of Science ®Google Scholar
• O’Toole EA, van Koningsveld R, Chen M, Woodley DT. Hypoxia induces epidermal keratinocyte matrix metalloproteinase-9 secretion via the protein kinase C pathway. J Cell Physiol. 2007;214:47–55. doi:10.1002/jcp.21160
   Web of Science ®Google Scholar
• Norman JT, Clark IM, Garcia PL. Regulation of TIMP-1 expression by hypoxia in kidney fibroblasts. Ann NY Acad Sci. 2006;878:503–505. doi:10.1111/j.1749-6632.1999.tb07709.x
   Google Scholar
• Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007;87:1285–1342. doi:10.1152/physrev.00012.2007
   PubMed Web of Science ®Google Scholar
• Liu W, Sood R, Chen Q, et al. Normobaric hyperoxia inhibits NADPH oxidase-mediated matrix metalloproteinase-9 induction in cerebral microvessels in experimental stroke. J Neurochem. 2008;107:1196–1205. doi:10.1111/j.1471-4159.2008.05664.x
   PubMed Web of Science ®Google Scholar
• Behn C, Araneda OF, Llanos AJ, Celedon G, Gonzalez G. Hypoxia-related lipid peroxidation: evidences, implications and approaches. Respir Physiol Neurobiol. 2007;158:143–150. doi:10.1016/j.resp.2007.06.001
   PubMed Web of Science ®Google Scholar
• Lesnefsky EJ, Chen Q, Slabe TJ, et al. Ischemia, rather than reperfusion, inhibits respiration through cytochrome oxidase in the isolated, perfused rabbit heart: role of cardiolipin. Amer J Physiol Heart Circ Physiol. 2004;287:H258–H267. doi:10.1152/ajpheart.00348.2003
   PubMed Web of Science ®Google Scholar
• Trush MA, Egner PA, Kensler TW. Myeloperoxidase as a biomarker of skin irritation and inflammation. Food Chem Toxicol. 1994;32:143–147. doi:10.1016/0278-6915(94)90175-9
   PubMed Web of Science ®Google Scholar
• McCord JM. Oxygen-derived radicals: a link between reperfusion and inflammation. Fed Proc. 1987;46:2402–2406.
   PubMedGoogle Scholar
• Angelos MG, Kutala VK, Torres CA, et al. Hypoxic reperfusion of the ischemic heart and oxygen radical generation. Am J Physiol Heart Circ Physiol. 2006;290:H341–H347. doi:10.1152/ajpheart.00223.2005
   PubMed Web of Science ®Google Scholar
• Stoner JD, Clanton TL, Aune SE, Angelos MG. O2 delivery and redox state are determinants of compartment-specific reactive O2 species in myocardial reperfusion. Am J Physiol Heart Circ Physiol. 2007;292:H109–H116. doi:10.1152/ajpheart.00925.2006
   PubMed Web of Science ®Google Scholar
• Thom SR. Oxidative stress is fundamental to hyperbaric oxygen therapy. J Appl Physiol. 2009;106:988–995. doi:10.1152/japplphysiol.91004.2008
   PubMed Web of Science ®Google Scholar
• Babchin A, Levich E, Melamed Y, Sivashinsky G. Osmotic phenomena in application for hyperbaric oxygen treatment. Colloids Surf B Biointerfaces. 2011;83:128–132. doi:10.1016/j.colsurfb.2010.11.019
   PubMed Web of Science ®Google Scholar
• Ziegler M, Wang X, Peter K. Platelets in cardiac ischaemia/reperfusion injury: a promising therapeutic target. Cardiovasc Res. 2019;115(7):1178–1188. doi:10.1093/cvr/cvz070
   PubMed Web of Science ®Google Scholar
• Hausenloy DJ, Botker HE, Engstrom T, et al. Targeting reperfusion injury in patients with ST-segment elevation myocardial infarction: trials and tribulations. Eur Heart J. 2017;38(13):935–941. doi:10.1093/eurheartj/ehw145
   PubMed Web of Science ®Google Scholar
• Davidson SM, Ferdinandy P, Andreadou I, et al. Multitarget strategies to reduce myocardial ischemia/reperfusion injury. J Am Coll Cardiol. 2019;73(1):89–99. doi:10.1016/j.jacc.2018.09.086
   PubMed Web of Science ®Google Scholar