The inflammatory response to extracorporeal membrane oxygenation (ECMO): a review of the pathophysiology

Critical Care - Tập 20 Số 1 - 2016
Jonathan Millar1, Jonathon P. Fanning1, Charles McDonald1, Daniel F. McAuley2, John F. Fraser1
1Critical Care Research Group, University of Queensland, Brisbane, Australia
2Wellcome-Wolfson Centre for Experimental Medicine, Queen’s University Belfast, Belfast, UK

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Hill JD, O'Brien TG, Murray JJ, Dontigny L, Bramson ML, Osborn JJ, Gerbode F. Prolonged extracorporeal oxygenation for acute post-traumatic respiratory failure (shock-lung syndrome). Use of the Bramson membrane lung. N Engl J Med. 1972;286(12):629–34.

Sauer CM, Yuh DD, Bonde P. Extracorporeal membrane oxygenation use has increased by 433% in adults in the United States from 2006 to 2011. ASAIO J. 2015;61(1):31–6.

Shekar K, Mullany DV, Thomson B, Ziegenfuss M, Platts DG, Fraser JF. Extracorporeal life support devices and strategies for management of acute cardiorespiratory failure in adult patients: a comprehensive review. Crit Care. 2014;18(3):219.

Mosier JM, Kelsey M, Raz Y, Gunnerson KJ, Meyer R, Hypes CD, Malo J, Whitmore SP, Spaite DW. Extracorporeal membrane oxygenation (ECMO) for critically ill adults in the emergency department: history, current applications, and future directions. Crit Care. 2015;19:431.

Schechter MA, Ganapathi AM, Englum BR, Speicher PJ, Daneshmand MA, Davis RD, Hartwig MG. Spontaneously breathing extracorporeal membrane oxygenation support provides the optimal bridge to lung transplantation. Transplantation. 2016;100(2):2699-2704.

Robinson S, Peek G. The role of ECMO in neonatal and paediatric patients. Paediatr Child Health. 2015;25(5):222–7.

Clark JB, Wang S, Palanzo DA, Wise R, Baer LD, Brehm C, Undar A. Current techniques and outcomes in extracorporeal life support. Artif Organs. 2015;39(11):926–30.

Gray BW, Haft JW, Hirsch JC, Annich GM, Hirschl RB, Bartlett RH. Extracorporeal life support: experience with 2,000 patients. ASAIO J. 2015;61(1):2–7.

Zangrillo A, Landoni G, Biondi-Zoccai G, Greco M, Greco T, Frati G, Patroniti N, Antonelli M, Pesenti A, Pappalardo F. A meta-analysis of complications and mortality of extracorporeal membrane oxygenation. Crit Care Resusc. 2013;15(3):172–8.

Tsai CW, Lin YF, Wu VC, Chu TS, Chen YM, Hu FC, Wu KD, Ko WJ. SAPS 3 at dialysis commencement is predictive of hospital mortality in patients supported by extracorporeal membrane oxygenation and acute dialysis. Eur J Cardiothorac Surg. 2008;34(6):1158–64.

Aubron C, Cheng AC, Pilcher D, Leong T, Magrin G, Cooper DJ, Scheinkestel C, Pellegrino V. Factors associated with outcomes of patients on extracorporeal membrane oxygenation support: a 5-year cohort study. Crit Care. 2013;17(2):R73.

Davies MG, Hagen PO. Systemic inflammatory response syndrome. Br J Surg. 1997;84(7):920–35.

Wang S, Krawiec C, Patel S, Kunselman AR, Song J, Lei F, Baer LD, Undar A. Laboratory evaluation of hemolysis and systemic inflammatory response in neonatal nonpulsatile and pulsatile extracorporeal life support systems. Artif Organs. 2015;39(9):774–81.

Rungatscher A, Tessari M, Stranieri C, Solani E, Linardi D, Milani E, Montresor A, Merigo F, Salvetti B, Menon T, et al. Oxygenator is the main responsible for leukocyte activation in experimental model of extracorporeal circulation: a cautionary tale. Mediators Inflamm. 2015;2015:484979.

McILwain RB, Timpa JG, Kurundkar AR, Holt DW, Kelly DR, Hartman YE, Neel ML, Karnatak RK, Schelonka RL, Anantharamaiah GM, et al. Plasma concentrations of inflammatory cytokines rise rapidly during ECMO-related SIRS due to the release of preformed stores in the intestine. Lab Invest. 2010;90(1):128–39.

Mildner RJ, Taub N, Vyas JR, Killer HM, Firmin RK, Field DJ, Kotecha S. Cytokine imbalance in infants receiving extracorporeal membrane oxygenation for respiratory failure. Biol Neonate. 2005;88(4):321–7.

Golej J, Winter P, Schoffmann G, Kahlbacher H, Stoll E, Boigner H, Trittenwein G. Impact of extracorporeal membrane oxygenation modality on cytokine release during rescue from infant hypoxia. Shock. 2003;20(2):110–5.

Adrian K, Mellgren K, Skogby M, Friberg LG, Mellgren G, Wadenvik H. Cytokine release during long-term extracorporeal circulation in an experimental model. Artif Organs. 1998;22(10):859–63.

Hirthler M, Simoni J, Dickson M. Elevated levels of endotoxin, oxygen-derived free radicals, and cytokines during extracorporeal membrane oxygenation. J Pediatr Surg. 1992;27(9):1199–202.

Graulich J, Sonntag J, Marcinkowski M, Bauer K, Kossel H, Buhrer C, Obladen M, Versmold HT. Complement activation by in vivo neonatal and in vitro extracorporeal membrane oxygenation. Mediators Inflamm. 2002;11(2):69–73.

Vallhonrat H, Swinford RD, Ingelfinger JR, Williams WW, Ryan DP, Tolkoff-Rubin N, Cosimi AB, Pascual M. Rapid activation of the alternative pathway of complement by extracorporeal membrane oxygenation. ASAIO J. 1999;45(1):113–4.

Moen O, Fosse E, Braten J, Andersson C, Fagerhol MK, Venge P, Hogasen K, Mollnes TE. Roller and centrifugal pumps compared in vitro with regard to haemolysis, granulocyte and complement activation. Perfusion. 1994;9(2):109–17.

Plotz FB, van Oeveren W, Bartlett RH, Wildevuur CR. Blood activation during neonatal extracorporeal life support. J Thorac Cardiovasc Surg. 1993;105(5):823–32.

Bergman P, Friberg G, Liu B, Al-Khaja N, Belboul A, Heideman M, Mellgren G, Roberts D. Blood cell rheologic deterioration by complement activation during experimental prolonged perfusion with membrane oxygenation. Perfusion. 1992;7(1):13–9.

Hocker JR, Wellhausen SR, Ward RA, Simpson PM, Cook LN. Effect of extracorporeal membrane oxygenation on leukocyte function in neonates. Artif Organs. 1991;15(1):23–8.

Graulich J, Walzog B, Marcinkowski M, Bauer K, Kossel H, Fuhrmann G, Buhrer C, Gaehtgens P, Versmold HT. Leukocyte and endothelial activation in a laboratory model of extracorporeal membrane oxygenation (ECMO). Pediatr Res. 2000;48(5):679–84.

Fortenberry JD, Bhardwaj V, Niemer P, Cornish JD, Wright JA, Bland L. Neutrophil and cytokine activation with neonatal extracorporeal membrane oxygenation. J Pediatr. 1996;128(5 Pt 1):670–8.

DePuydt LE, Schuit KE, Smith SD. Effect of extracorporeal membrane oxygenation on neutrophil function in neonates. Crit Care Med. 1993;21(9):1324–7.

Adib-Conquy M, Cavaillon JM. Compensatory anti-inflammatory response syndrome. Thromb Haemost. 2009;101(1):36–47.

Shi J, Chen Q, Yu W, Shen J, Gong J, He C, Hu Y, Zhang J, Gao T, Xi F, et al. Continuous renal replacement therapy reduces the systemic and pulmonary inflammation induced by venovenous extracorporeal membrane oxygenation in a porcine model. Artif Organs. 2014;38(3):215–23.

He C, Yang S, Yu W, Chen Q, Shen J, Hu Y, Shi J, Wu X, Li J, Li N. Effects of continuous renal replacement therapy on intestinal mucosal barrier function during extracorporeal membrane oxygenation in a porcine model. J Cardiothorac Surg. 2014;9:72.

Yimin H, Wenkui Y, Jialiang S, Qiyi C, Juanhong S, Zhiliang L, Changsheng H, Ning L, Jieshou L. Effects of continuous renal replacement therapy on renal inflammatory cytokines during extracorporeal membrane oxygenation in a porcine model. J Cardiothorac Surg. 2013;8:113.

Shen J, Yu W, Chen Q, Shi J, Hu Y, Zhang J, Gao T, Xi F, He C, Gong J, et al. Continuous renal replacement therapy (CRRT) attenuates myocardial inflammation and mitochondrial injury induced by venovenous extracorporeal membrane oxygenation (VV ECMO) in a healthy piglet model. Inflammation. 2013;36(5):1186–93.

Shen J, Yu W, Shi J, Chen Q, Hu Y, Zhang J, Gao T, Xi F, Gong J, He C, et al. Effect of venovenous extracorporeal membrane oxygenation on the heart in a healthy piglet model. J Cardiothorac Surg. 2013;8:163.

Chen Q, Yu W, Shi J, Shen J, Hu Y, Gao T, Zhang J, Xi F, Gong J, Li J, et al. The effect of venovenous extra-corporeal membrane oxygenation (ECMO) therapy on immune inflammatory response of cerebral tissues in porcine model. J Cardiothorac Surg. 2013;8:186.

Warren OJ, Smith AJ, Alexiou C, Rogers PL, Jawad N, Vincent C, Darzi AW, Athanasiou T. The inflammatory response to cardiopulmonary bypass: part 1–mechanisms of pathogenesis. J Cardiothorac Vasc Anesth. 2009;23(2):223–31.

Warren OJ, Watret AL, de Wit KL, Alexiou C, Vincent C, Darzi AW, Athanasiou T. The inflammatory response to cardiopulmonary bypass: part 2–anti-inflammatory therapeutic strategies. J Cardiothorac Vasc Anesth. 2009;23(3):384–93.

Landis RC, Brown JR, Fitzgerald D, Likosky DS, Shore-Lesserson L, Baker RA, Hammon JW. Attenuating the systemic inflammatory response to adult cardiopulmonary bypass: a critical review of the evidence base. J Extra Corpor Technol. 2014;46(3):197–211.

Sniecinski RM, Levy JH. Anticoagulation management associated with extracorporeal circulation. Best Pract Res Clin Anaesthesiol. 2015;29(2):189–202.

Esper SA, Levy JH, Waters JH, Welsby IJ. Extracorporeal membrane oxygenation in the adult: a review of anticoagulation monitoring and transfusion. Anesth Analg. 2014;118(4):731–43.

Pagowska-Klimek I, Swierzko AS, Michalski M, Glowacka E, Szala-Pozdziej A, Sokolowska A, Moll M, Krajewski WR, Romak J, Cedzynski M. Activation of the lectin pathway of complement by cardiopulmonary bypass contributes to the development of systemic inflammatory response syndrome after pediatric cardiac surgery. Clin Exp Immunol. 2015;184(2):257–63.

Schaub C, Thomas OD, Åkervall Fridh L, Schött U. Protamine dosage effects on complement activation and sonoclot coagulation analysis after cardiac surgery. Cardiovasc Syst. 2013;1(1). http://dx.doi.org/10.7243/2052-4358-1-1 .

DeFoe GR, Ross CS, Olmstead EM, Surgenor SD, Fillinger MP, Groom RC, Forest RJ, Pieroni JW, Warren CS, Bogosian ME, et al. Lowest hematocrit on bypass and adverse outcomes associated with coronary artery bypass grafting. Northern New England Cardiovascular Disease Study Group. Ann Thorac Surg. 2001;71(3):769–76.

Gourlay T, Samartzis I, Taylor KM. The effect of haemodilution on blood-biomaterial contact-mediated CD11b expression on neutrophils: ex vivo studies. Perfusion. 2003;18(2):87–93.

Gäbel J, Westerberg M, Bengtsson A, Jeppsson A. Cell salvage of cardiotomy suction blood improves the balance between pro- and anti-inflammatory cytokines after cardiac surgery. Eur J Cardiothorac Surg. 2013;44(3):506–11.

Westerberg M, Bengtsson A, Jeppsson A. Coronary surgery without cardiotomy suction and autotransfusion reduces the postoperative systemic inflammatory response. Ann Thorac Surg. 2004;78(1):54–9.

Damgaard S, Nielsen CH, Andersen LW, Bendtzen K, Tvede M, Steinbruchel DA. Cell saver for on-pump coronary operations reduces systemic inflammatory markers: a randomized trial. Ann Thorac Surg. 2010;89(5):1511–7.

Ji B, Ündar A. An evaluation of the benefits of pulsatile versus nonpulsatile perfusion during cardiopulmonary bypass procedures in pediatric and adult cardiac patients. ASAIO J. 2006;52(4):357–61.

Massoudy P, Zahler S, Becker BF, Braun SL, Barankay A, Meisner H. Evidence for inflammatory responses of the lungs during coronary artery bypass grafting with cardiopulmonary bypass. Chest. 2001;119(1):31–6.

Orime Y, Shiono M, Hata H, Yagi S, Tsukamoto S, Okumura H, Nakata K, Kimura S, Hata M, Sezai A, et al. Cytokine and endothelial damage in pulsatile and nonpulsatile cardiopulmonary bypass. Artif Organs. 1999;23(6):508–12.

O'Neill B, McDowell K, Bradley J, Blackwood B, Mullan B, Lavery G, Agus A, Murphy S, Gardner E, McAuley DF. Effectiveness of a programme of exercise on physical function in survivors of critical illness following discharge from the ICU: study protocol for a randomised controlled trial (REVIVE). Trials. 2014;15:146.

den Hengst WA, Gielis JF, Lin JY, Van Schil PE, De Windt LJ, Moens AL. Lung ischemia-reperfusion injury: a molecular and clinical view on a complex pathophysiological process. Am J Physiol Heart Circ Physiol. 2010;299(5):H1283–99.

Wendel HP, Scheule AM, Eckstein FS, Ziemer G. Haemocompatibility of paediatric membrane oxygenators with heparin-coated surfaces. Perfusion. 1999;14(1):21–8.

Wachtfogel YT, Hack CE, Nuijens JH, Kettner C, Reilly TM, Knabb RM, Bischoff R, Tschesche H, Wenzel H, Kucich U, et al. Selective kallikrein inhibitors alter human neutrophil elastase release during extracorporeal circulation. Am J Phys. 1995;268(3 Pt 2):H1352–7.

Larsson M, Rayzman V, Nolte MW, Nickel KF, Björkqvist J, Jämsä A, Hardy MP, Fries M, Schmidbauer S, Hedenqvist P, et al. A factor XIIa inhibitory antibody provides thromboprotection in extracorporeal circulation without increasing bleeding risk. Sci Transl Med. 2014;6((222):222ra217.

Rodell TC, Naidoo Y, Bhoola KD. Role of kinins in inflammatory responses. Clin Immunotherapeutics. 2012;3(5):352–61.

Cugno M, Nussberger J, Biglioli P, Giovagnoni MG, Gardinali M, Agostoni A. Cardiopulmonary bypass increases plasma bradykinin concentrations. Immunopharmacology. 1999;43(2–3):145–7.

Morgan EN, Pohlman TH, Vocelka C, Farr A, Lindley G, Chandler W, Griscavage-Ennis JM, Verrier ED. Nuclear factor κB mediates a procoagulant response in monocytes during extracorporeal circulation. J Thorac Cardiovasc Surg. 2003;125(1):165–71.

Kappelmayer J, Bernabei A, Edmunds LH, Edgington TS, Colman RW. Tissue factor is expressed on monocytes during simulated extracorporeal circulation. Circ Res. 1993;72(5):1075–81.

Barstad RM, ØVrum E, Ringdal M-AL, ØYstese R, Hamers MJAG, Veiby OP, Rolfsen T, Stephens RW, Sakariassen KS. Induction of monocyte tissue factor procoagulant activity during coronary artery bypass surgery is reduced with heparin-coated extracorporeal circuit. Br J Haematol. 1996;94(3):517–25.

Szotowski B, Antoniak S, Poller W, Schultheiss H-P, Rauch U. Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res. 2005;96(12):1233–9.

Kaplanski G, Fabrigoule M, Boulay V, Dinarello CA, Bongrand P, Kaplanski S, Farnarier C. Thrombin induces endothelial type II activation in vitro: IL-1 and TNF-alpha-independent IL-8 secretion and E-selectin expression. J Immunol. 1997;158(11):5435–41.

Zimmerman GA, McIntyre TM, Prescott SM. Thrombin stimulates the adherence of neutrophils to human endothelial cells in vitro. J Clin Investig. 1985;76(6):2235–46.

Prescott SM, Zimmerman GA, McIntyre TM. Human endothelial cells in culture produce platelet-activating factor (1-alkyl-2-acetyl-sn-glycero-3-phosphocholine) when stimulated with thrombin. Proc Natl Acad Sci USA. 1984;81(11):3534–8.

Levy JH, Tanaka KA. Inflammatory response to cardiopulmonary bypass. Ann Thorac Surg. 2003;75(2):S715–20.

Rahe-Meyer N, Solomon C, Tokuno ML, Winterhalter M, Shrestha M, Hahn A, Tanaka K. Comparative assessment of coagulation changes induced by two different types of heart-lung machine. Artif Organs. 2010;34(1):3–12.

Fromes Y, Gaillard D, Ponzio O, Chauffert M, Gerhardt MF, Deleuze P, Bical OM. Reduction of the inflammatory response following coronary bypass grafting with total minimal extracorporeal circulation. Eur J Cardiothorac Surg. 2002;22(4):527–33.

Cheung PY, Sawicki G, Salas E, Etches PC, Schulz R, Radomski MW. The mechanisms of platelet dysfunction during extracorporeal membrane oxygenation in critically ill neonates. Crit Care Med. 2000;28(7):2584–90.

Sims PJ, Wiedmer T. The response of human platelets to activated components of the complement system. Immunol Today. 1991;12(9):338–42.

Whiteheart SW. Platelet granules: surprise packages. Blood. 2011;118(5):1190–1.

Kraft F, Schmidt C, Van Aken H, Zarbock A. Inflammatory response and extracorporeal circulation. Best Pract Res Clin Anaesthesiol. 2015;29(2):113–23.

Rinder H, Bonan J, Rinder C, Ault K, Smith B. Activated and unactivated platelet adhesion to monocytes and neutrophils. Blood. 1991;78(7):1760–9.

Neumann FJ, Marx N, Gawaz M, Brand K, Ott I, Rokitta C, Sticherling C, Meinl C, May A, Schomig A. Induction of cytokine expression in leukocytes by binding of thrombin-stimulated platelets. Circulation. 1997;95(10):2387–94.

Maugeri N, Brambilla M, Camera M, Carbone A, Tremoli E, Donati MB, De Gaetano G, Cerletti C. Human polymorphonuclear leukocytes produce and express functional tissue factor upon stimulation1. J Thromb Haemost. 2006;4(6):1323–30.

Dunkelberger JR, Song W-C. Complement and its role in innate and adaptive immune responses. Cell Res. 2009;20(1):34–50.

Ricklin D, Lambris JD. Complement in immune and inflammatory disorders: pathophysiological mechanisms. J Immunol. 2013;190(8):3831–8.

Nilsson B, Ekdahl KN, Mollnes TE, Lambris JD. The role of complement in biomaterial-induced inflammation. Mol Immunol. 2007;44(1-3):82–94.

Ascione R, Lloyd CT, Underwood MJ, Lotto AA, Pitsis AA, Angelini GD. Inflammatory response after coronary revascularization with or without cardiopulmonary bypass. Ann Thorac Surg. 2000;69(4):1198–204.

Johansson-Synnergren M, Nilsson F, Bengtsson A, Jeppsson A, Wiklund L. Off-pump CABG reduces complement activation but does not significantly affect peripheral endothelial function: a prospective randomized study. Scand Cardiovasc J. 2004;38(1):53–8.

Wehlin L, Vedin J, Vaage J, Lundahl J. Activation of complement and leukocyte receptors during on- and off pump coronary artery bypass surgery. Eur J Cardiothorac Surg. 2004;25(1):35–42.

Struber M, Cremer JT, Gohrbandt B, Hagl C, Jankowski M, Volker B, Ruckoldt H, Martin M, Haverich A. Human cytokine responses to coronary artery bypass grafting with and without cardiopulmonary bypass. Ann Thorac Surg. 1999;68(4):1330–5.

Lindholm L, Westerberg M, Bengtsson A, Ekroth R, Jensen E, Jeppsson A. A closed perfusion system with heparin coating and centrifugal pump improves cardiopulmonary bypass biocompatibility in elderly patients. Ann Thorac Surg. 2004;78(6):2131–8. discussion 2138.

Morgan IS, Codispoti M, Sanger K, Mankad PS. Superiority of centrifugal pump over roller pump in paediatric cardiac surgery: prospective randomised trial. Eur J Cardiothorac Surg. 1998;13(5):526–32.

Hein E, Munthe-Fog L, Thiara AS, Fiane AE, Mollnes TE, Garred P. Heparin-coated cardiopulmonary bypass circuits selectively deplete the pattern recognition molecule ficolin-2 of the lectin complement pathway in vivo. Clin Exp Immunol. 2015;179(2):294–9.

Ware LB, Eisner MD, Thompson BT, Parsons PE, Matthay MA. Significance of von Willebrand factor in septic and nonseptic patients with acute lung injury. Am J Respir Crit Care Med. 2004;170(7):766–72.

Duffy MJ, Mullan BA, Craig TR, Shyamsundar M, MacSweeney RE, Thompson G, Stevenson M, McAuley DF. Impaired endothelium-dependent vasodilatation is a novel predictor of mortality in intensive care. Crit Care Med. 2011;39(4):629–35.

Boyle Jr EM, Pohlman TH, Johnson MC, Verrier ED. Endothelial cell injury in cardiovascular surgery: the systemic inflammatory response. Ann Thorac Surg. 1997;63(1):277–84.

Fischetti F, Tedesco F. Cross-talk between the complement system and endothelial cells in physiologic conditions and in vascular diseases. Autoimmunity. 2006;39(5):417–28.

Perkins GD, Nathani N, McAuley DF, Gao F, Thickett DR. In vitro and in vivo effects of salbutamol on neutrophil function in acute lung injury. Thorax. 2007;62(1):36–42.

Wachtfogel YT, Kucich U, Hack CE, Gluszko P, Niewiarowski S, Colman RW, Edmunds Jr LH. Aprotinin inhibits the contact, neutrophil, and platelet activation systems during simulated extracorporeal perfusion. J Thorac Cardiovasc Surg. 1993;106(1):1–9. discussion 9-10.

Rinder CS, Rinder HM, Smith BR, Fitch JC, Smith MJ, Tracey JB, Matis LA, Squinto SP, Rollins SA. Blockade of C5a and C5b-9 generation inhibits leukocyte and platelet activation during extracorporeal circulation. J Clin Investig. 1995;96(3):1564–72.

Kruger P, Saffarzadeh M, Weber AN, Rieber N, Radsak M, von Bernuth H, Benarafa C, Roos D, Skokowa J, Hartl D. Neutrophils: Between host defence, immune modulation, and tissue injury. PLoS Pathog. 2015;11(3):e1004651.

Kotani N, Hashimoto H, Sessler DI, Muraoka M, Wang JS, O'Connor MF, Matsuki A. Neutrophil number and interleukin-8 and elastase concentrations in bronchoalveolar lavage fluid correlate with decreased arterial oxygenation after cardiopulmonary bypass. Anesth Analg. 2000;90(5):1046–51.

Brix-Christensen V, Tonnesen E, Hjortdal VE, Chew M, Flo C, Marqversen J, Hansen JF, Andersen NT, Ravn HB. Neutrophils and platelets accumulate in the heart, lungs, and kidneys after cardiopulmonary bypass in neonatal pigs. Crit Care Med. 2002;30(3):670–6.

Kiaii B, Fox S, Swinamer SA, Rayman R, Higgins J, Cleland A, Fernandes P, MacDonald J, Dobkowski WB, Stitt LW, et al. The early inflammatory response in a mini-cardiopulmonary bypass system: a prospective randomized study. Innovations (Phila). 2012;7(1):23–32.

Bergman P, Belboul A, Göran Friberg L, Al-Khaja N, Mellgren G, Roberts D. The effect of prolonged perfusion with a membrane oxygenator (PPMO) on white blood cells. Perfusion. 1994;9(1):35–40.

van Furth R. Human monocytes and cytokines. Res Immunol. 1998;149(7–8):719–20.

Moore Jr FD, Socher SH, Davis C. Tumor necrosis factor and endotoxin can cause neutrophil activation through separate pathways. Arch Surg. 1991;126(1):70–3.

Bradley JR. TNF-mediated inflammatory disease. J Pathol. 2008;214(2):149–60.

Jones SA, Hooriuchi S, Topley N, Yamamoto N, Fuller GM. The soluble interleukin 6 receptor: mechanisms of production and implications in disease. FASEB J. 2001;15(1):43–58.

Jialiang S, Juanhong S, Qiyi C, Wenkui Y, Changsheng H, Yimin H, Juanjuan Z, Tao G, Fengchan X, Jieshou L. In-line hemofiltration minimized extracorporeal membrane oxygenation-related inflammation in a porcine model. Perfusion. 2014;29(6):526–33.

Risnes I, Wagner K, Ueland T, Mollnes T, Aukrust P, Svennevig J. Interleukin-6 may predict survival in extracorporeal membrane oxygenation treatment. Perfusion. 2008;23(3):173–8.

Hong TH, Kuo SW, Hu FC, Ko WJ, Hsu LM, Huang SC, Yang YW, Yu SL, Chen YS. Do interleukin-10 and superoxide ions predict outcomes of cardiac extracorporeal membrane oxygenation patients? Antioxid Redox Signal. 2014;20(1):60–8.

Bartlett RH. ECMO: The next ten years. Egyptian J Crit Care Med. 2016;4(1):7–10.

Kenne E, Renné T. Factor XII: a drug target for safe interference with thrombosis and inflammation. Drug Discov Today. 2014;19(9):1459–64.

Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143–7.

Le Blanc K, Davies LC. Mesenchymal stromal cells and the innate immune response. Immunol Lett. 2015;168(2):140–6.

Qiang Y, Liang G, Yu L. Human amniotic mesenchymal stem cells alleviate lung injury induced by ischemia and reperfusion after cardiopulmonary bypass in dogs. Lab Invest. 2016;96(5):537–46.

Clive Landis R, Murkin JM, Stump DA, Baker RA, Arrowsmith JE, De Somer F, Dain SL, Dobkowski WB, Ellis JE, Falter F, et al. Consensus statement: minimal criteria for reporting the systemic inflammatory response to cardiopulmonary bypass. Heart Surg Forum. 2010;13(2):E116–23.