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Extracorporeal Circulation-Related Immune Response

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Management of Dysregulated Immune Response in the Critically Ill

Part of the book series: Lessons from the ICU ((LEICU))

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Abstract

Forms of extracorporeal circulation are increasingly used to support critically ill patients. Extracorporeal membrane oxygenation (ECMO) and renal replacement therapy (RRT) are two of the most widely used and are employed as bridges to recovery or as definitive therapy. While both are life-saving, they also have limitations. Of note, ECMO and RRT have been associated with dysregulation of the immune system. Both are known to trigger a pro-inflammatory response; alter leukocyte numbers, phenotype, and function; increase platelet/endothelial-leukocyte interplay; and lead to a pro-coagulant state, alongside some features of immunosuppression. These changes may be exacerbated by blood contacting non-endothelialised surfaces as well as the non-physiological conditions associated with these modalities. However, teasing out the immune effects caused by these modalities from the actual underlying disease burden is complex. This chapter describes and highlights the immune responses related to extracorporeal circulations. Additionally, it outlines the factors contributing to ECMO- and RRT-related immune dysregulation, and the role these changes play in device complications. An increased understanding and acknowledgement of the patient-pump and -oxygenator interphase may assist in guiding the design of targeted preventative actions in the future.

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References

  1. Karkar A. Advances in hemodialysis techniques. 2013 [cited Oct 2021, date last access)]. In: Hemodialysis [Internet]. http://www.intechopen.com/books/hemodialysis/advances-in-hemodialysis-techniques. IntechOpen, [cited Oct 2021, date last access)].

  2. Himmelfarb J, Vanholder R, Mehrotra R, Tonelli M. The current and future landscape of dialysis. Nat Rev Nephrol. 2020;16(10):573–85.

    PubMed  PubMed Central  Google Scholar 

  3. Damasiewicz MJ, Polkinghorne KR. Global dialysis perspective: Australia. Kidney360. 2020;1(1):48–51.

    PubMed  PubMed Central  Google Scholar 

  4. Prowle JR, Bellomo R. Continuous renal replacement therapy: recent advances and future research. Nat Rev Nephrol. 2010;6(9):521–9.

    PubMed  Google Scholar 

  5. Hsu RK, McCulloch CE, Dudley RA, Lo LJ, Hsu CY. Temporal changes in incidence of dialysis-requiring AKI. J Am Soc Nephrol. 2013;24(1):37–42.

    PubMed  Google Scholar 

  6. Hoste EA, Bagshaw SM, Bellomo R, Cely CM, Colman R, Cruz DN, et al. Epidemiology of acute kidney injury in critically ill patients: the multinational AKI-EPI study. Intensive Care Med. 2015;41(8):1411–23.

    PubMed  Google Scholar 

  7. Ahmed AR, Obilana A, Lappin D. Renal replacement therapy in the critical care setting. Crit Care Res Pract. 2019;2019:6948710.

    PubMed  PubMed Central  Google Scholar 

  8. Marshall MR, Ma T, Galler D, Rankin APN, Williams AB. Sustained low-efficiency daily diafiltration (SLEDD-f) for critically ill patients requiring renal replacement therapy: towards an adequate therapy. Nephrol Dial Transplant. 2004;19(4):877–84.

    PubMed  Google Scholar 

  9. Kihara M, Ikeda Y, Shibata K, Masumori S, Fujita H, Ebira H, et al. Slow hemodialysis performed during the day in managing renal failure in critically ill patients. Nephron. 1994;67(1):36–41.

    CAS  PubMed  Google Scholar 

  10. Marshall MR, Golper TA, Shaver MJ, Alam MG, Chatoth DK. Sustained low-efficiency dialysis for critically ill patients requiring renal replacement therapy. Kidney Int. 2001;60(2):777–85.

    CAS  PubMed  Google Scholar 

  11. Trahanas JM, Kolobow MA, Hardy MA, Berra L, Zapol WM, Bartlett RH. “Treating lungs”: the scientific contributions of Dr. Theodor Kolobow. ASAIO J. 2016;62(2):203–10.

    PubMed  PubMed Central  Google Scholar 

  12. Kolobow T. The promise of the membrane artificial lung. Int J Artif Organs. 1978;1(1):15–20.

    CAS  PubMed  Google Scholar 

  13. Lequier L, Horton SB, McMullan DM, Bartlett RH. Extracorporeal membrane oxygenation circuitry. Pediatr Crit Care Med. 2013;14(5 Suppl 1):S7–S12.

    PubMed  PubMed Central  Google Scholar 

  14. Peek GJ, Elbourne D, Mugford M, Tiruvoipati R, Wilson A, Allen E, et al. Randomised controlled trial and parallel economic evaluation of conventional ventilatory support versus extracorporeal membrane oxygenation for severe adult respiratory failure (CESAR). Health Technol Assess. 2010;14(35):1–46.

    CAS  PubMed  Google Scholar 

  15. Combes A, Hajage D, Capellier G, Demoule A, Lavoue S, Guervilly C, et al. Extracorporeal membrane oxygenation for severe acute respiratory distress syndrome. N Engl J Med. 2018;378(21):1965–75.

    PubMed  Google Scholar 

  16. Davies A, Jones D, Bailey M, Beca J, Bellomo R, Blackwell N, et al. Extracorporeal membrane oxygenation for 2009 influenza A(H1N1) acute respiratory distress syndrome. JAMA. 2009;302(17):1888–95.

    CAS  PubMed  Google Scholar 

  17. Zangrillo A, Biondi-Zoccai G, Landoni G, Frati G, Patroniti N, Pesenti A, et al. Extracorporeal membrane oxygenation (ECMO) in patients with H1N1 influenza infection: a systematic review and meta-analysis including 8 studies and 266 patients receiving ECMO. Crit Care. 2013;17(1):R30.

    PubMed  PubMed Central  Google Scholar 

  18. Extracorporeal Life Support Organization. ECLS registry report: international summary 2019. Ann Arbor; 2019.

    Google Scholar 

  19. Fraser JF, Shekar K, Diab S, Dunster K, Foley SR, McDonald CI, et al. ECMO—the clinician’s view. ISBT Sci Ser. 2012;7(1):82–8.

    Google Scholar 

  20. Makdisi G, Wang IW. Extra corporeal membrane oxygenation (ECMO) review of a lifesaving technology. J Thorac Dis. 2015;7(7):E166–76.

    PubMed  PubMed Central  Google Scholar 

  21. MacLaren G, Schlapbach LJ, Aiken AM. Nosocomial infections during extracorporeal membrane oxygenation in neonatal, pediatric, and adult patients: a comprehensive narrative review. Pediatr Crit Care Med. 2020;21(3):283–90.

    PubMed  Google Scholar 

  22. Li PK-T, Chow KM. Infectious complications in dialysis—epidemiology and outcomes. Nat Rev Nephrol. 2012;8(2):77–88.

    CAS  Google Scholar 

  23. Parienti J-J, Dugué AE, Daurel C, Mira J-P, Mégarbane B, Mermel LA, et al. Continuous renal replacement therapy may increase the risk of catheter infection. Clin J Am Soc Nephrol. 2010;5(8):1489–96.

    PubMed  PubMed Central  Google Scholar 

  24. Dalton HJ, Reeder R, Garcia-Filion P, Holubkov R, Berg RA, Zuppa A, et al. Factors associated with bleeding and thrombosis in children receiving extracorporeal membrane oxygenation. Am J Respir Crit Care Med. 2017;196(6):762–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Braune S, Sieweke A, Brettner F, Staudinger T, Joannidis M, Verbrugge S, et al. The feasibility and safety of extracorporeal carbon dioxide removal to avoid intubation in patients with COPD unresponsive to noninvasive ventilation for acute hypercapnic respiratory failure (ECLAIR study): multicentre case–control study. Intensive Care Med. 2016;42(9):1437–44.

    CAS  PubMed  Google Scholar 

  26. Sklar MC, Beloncle F, Katsios CM, Brochard L, Friedrich JO. Extracorporeal carbon dioxide removal in patients with chronic obstructive pulmonary disease: a systematic review. Intensive Care Med. 2015;41(10):1752–62.

    CAS  PubMed  Google Scholar 

  27. Peperstraete H, Eloot S, Depuydt P, De Somer F, Roosens C, Hoste E. Low flow extracorporeal CO(2) removal in ARDS patients: a prospective short-term crossover pilot study. BMC Anesthesiol. 2017;17(1):155.

    PubMed  PubMed Central  Google Scholar 

  28. Thongprayoon C, Cheungpasitporn W, Lertjitbanjong P, Aeddula NR, Bathini T, Watthanasuntorn K, et al. Incidence and impact of acute kidney injury in patients receiving extracorporeal membrane oxygenation: a meta-analysis. J Clin Med. 2019;8(7):981.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Larsson M, Rayzman V, Nolte MW, Nickel KF, Björkqvist J, Jämsä A, et al. A factor XIIa inhibitory antibody provides thromboprotection in extracorporeal circulation without increasing bleeding risk. Sci Transl Med. 2014;6(222):222ra17.

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  31. 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.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  33. Frank RD, Weber J, Dresbach H, Thelen H, Weiss C, Floege J. Role of contact system activation in hemodialyzer-induced thrombogenicity. Kidney Int. 2001;60(5):1972–81.

    CAS  PubMed  Google Scholar 

  34. François K, Orlando C, Jochmans K, Cools W, De Meyer V, Tielemans C, et al. Hemodialysis does not induce detectable activation of the contact system of coagulation. Kidney Int Rep. 2020;5(6):831–8.

    PubMed  PubMed Central  Google Scholar 

  35. 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.

    CAS  PubMed  Google Scholar 

  36. Rodell TC, Naidoo Y, Bhoola KD. Role of kinins in inflammatory responses. Clin Immunotherap. 1995;3(5):352–61.

    Google Scholar 

  37. Marney AM, Ma J, Luther JM, Ikizler TA, Brown NJ. Endogenous bradykinin contributes to increased plasminogen activator inhibitor 1 antigen following hemodialysis. J Am Soc Nephrol. 2009;20(10):2246–52.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Morgan EN, Pohlman TH, Vocelka C, Farr A, Lindley G, Chandler W, et al. Nuclear factor kappaB mediates a procoagulant response in monocytes during extracorporeal circulation. J Thorac Cardiovasc Surg. 2003;125(1):165–71.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  40. Ocak G, Vossen CY, Rotmans JI, Lijfering WM, Rosendaal FR, Parlevliet KJ, et al. Venous and arterial thrombosis in dialysis patients. Thromb Haemost. 2011;106(6):1046–52.

    CAS  PubMed  Google Scholar 

  41. Oudemans-van Straaten HM. Hemostasis and thrombosis in continuous renal replacement treatment. Semin Thromb Hemost. 2015;41(1):91–8.

    CAS  PubMed  Google Scholar 

  42. Skinner SC, Derebail VK, Poulton CJ, Bunch DC, Roy-Chaudhury P, Key NS. Hemodialysis-related complement and contact pathway activation and cardiovascular risk: a narrative review. Kidney Med. 2021;3(4):607–18.

    PubMed  PubMed Central  Google Scholar 

  43. Lappegård KT, Christiansen D, Pharo A, Thorgersen EB, Hellerud BC, Lindstad J, et al. Human genetic deficiencies reveal the roles of complement in the inflammatory network: lessons from nature. Proc Natl Acad Sci U S A. 2009;106(37):15861–6.

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  45. Graulich J, Sonntag J, Marcinkowski M, Bauer K, Kössel H, Bührer C, et al. Complement activation by in vivo neonatal and in vitro extracorporeal membrane oxygenation. Mediat Inflamm. 2002;11(2):69–73.

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  47. Poppelaars F, da Costa MG, Faria B, Berger SP, Assa S, Daha MR, et al. Intradialytic complement activation precedes the development of cardiovascular events in hemodialysis patients. Front Immunol. 2018;9:2070.

    PubMed  PubMed Central  Google Scholar 

  48. Lhotta K, Würzner R, Kronenberg F, Oppermann M, König P. Rapid activation of the complement system by cuprophane depends on complement component C4. Kidney Int. 1998;53(4):1044–51.

    CAS  PubMed  Google Scholar 

  49. Inoshita H, Ohsawa I, Kusaba G, Ishii M, Onda K, Horikoshi S, et al. Complement in patients receiving maintenance hemodialysis: functional screening and quantitative analysis. BMC Nephrol. 2010;11:34.

    PubMed  PubMed Central  Google Scholar 

  50. 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Burnouf T, Eber M, Kientz D, Cazenave JP, Burkhardt T. Assessment of complement activation during membrane-based plasmapheresis procedures. J Clin Apher. 2004;19(3):142–7.

    PubMed  Google Scholar 

  52. Eskandary F, Wahrmann M, Biesenbach P, Sandurkov C, König F, Schwaiger E, et al. ABO antibody and complement depletion by immunoadsorption combined with membrane filtration—a randomized, controlled, cross-over trial. Nephrol Dial Transplant. 2014;29(3):706–14.

    CAS  PubMed  Google Scholar 

  53. Chenoweth DE, Cheung AK, Henderson LW. Anaphylatoxin formation during hemodialysis: effects of different dialyzer membranes. Kidney Int. 1983;24(6):764–9.

    CAS  PubMed  Google Scholar 

  54. Stasi A, Franzin R, Divella C, Sallustio F, Curci C, Picerno A, et al. PMMA-based continuous hemofiltration modulated complement activation and renal dysfunction in LPS-induced acute kidney injury. Front Immunol. 2021;12:605212.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  56. Ki KK, Passmore MR, Chan CHH, Malfertheiner MV, Bouquet M, Cho HJ, et al. Effect of ex vivo extracorporeal membrane oxygenation flow dynamics on immune response. Perfusion. 2019;34(1_suppl):5–14.

    PubMed  Google Scholar 

  57. Schindler R, Linnenweber S, Schulze M, Oppermann M, Dinarello CA, Shaldon S, et al. Gene expression of interleukin-1 beta during hemodialysis. Kidney Int. 1993;43(3):712–21.

    CAS  PubMed  Google Scholar 

  58. 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.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  60. 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):670–8.

    CAS  PubMed  Google Scholar 

  61. Passmore MR, Fung YL, Simonova G, Foley SR, Dunster KR, Diab SD, et al. Inflammation and lung injury in an ovine model of extracorporeal membrane oxygenation support. Am J Physiol Lung Cell Mol Physiol. 2016;311(6):L1202–12.

    PubMed  Google Scholar 

  62. McIlwain RB, Timpa JG, Kurundkar AR, Holt DW, Kelly DR, Hartman YE, 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.

    CAS  PubMed  Google Scholar 

  63. Rungatscher A, Tessari M, Stranieri C, Solani E, Linardi D, Milani E, et al. Oxygenator is the main responsible for leukocyte activation in experimental model of extracorporeal circulation: a cautionary tale. Mediat Inflamm. 2015;2015:7.

    Google Scholar 

  64. Caglar K, Peng Y, Pupim LB, Flakoll PJ, Levenhagen D, Hakim RM, et al. Inflammatory signals associated with hemodialysis. Kidney Int. 2002;62(4):1408–16.

    CAS  PubMed  Google Scholar 

  65. Servillo G, Vargas M, Pastore A, Procino A, Iannuzzi M, Capuano A, et al. Immunomodulatory effect of continuous venovenous hemofiltration during sepsis: preliminary data. Biomed Res Int. 2013;2013:108951.

    PubMed  PubMed Central  Google Scholar 

  66. Yong K, Dogra G, Boudville N, Lim W. Increased inflammatory response in association with the initiation of hemodialysis compared with peritoneal dialysis in a prospective study of end-stage kidney disease patients. Perit Dial Int. 2018;38(1):18–23.

    CAS  PubMed  Google Scholar 

  67. Adrian K, Skogby M, Friberg LG, Mellgren K. The effect of s-nitroso-glutathione on platelet and leukocyte function during experimental extracorporeal circulation. Artif Organs. 2003;27(6):570–5.

    CAS  PubMed  Google Scholar 

  68. Lisowska KA, Pindel M, Pietruczuk K, Kuźmiuk-Glembin I, Storoniak H, Dębska-Ślizień A, et al. The influence of a single hemodialysis procedure on human T lymphocytes. Sci Rep. 2019;9(1):5041.

    PubMed  PubMed Central  Google Scholar 

  69. Borazan A, Ustün H, Ustundag Y, Aydemir S, Bayraktaroglu T, Sert M, et al. The effects of peritoneal dialysis and hemodialysis on serum tumor necrosis factor-alpha, interleukin-6, interleukin-10 and C-reactive-protein levels. Mediat Inflamm. 2004;13(3):201–4.

    CAS  Google Scholar 

  70. Ziemba K, Nateri J, Hanson-Huber L, Steele L, Cismowski M, West T, et al. Innate and adaptive immune function during extracorporeal membrane oxygenation. Crit Care Med. 2016;44(12):232.

    Google Scholar 

  71. Beshish AG, Bradley JD, McDonough KL, Halligan NLN, McHugh WM, Sturza J, et al. The functional immune response of patients on extracorporeal life support. ASAIO J. 2018;65(1):77–83.

    Google Scholar 

  72. Li G, Ma H, Yin Y, Wang J. CRP, IL-2 and TNF-α level in patients with uremia receiving hemodialysis. Mol Med Rep. 2018;17(2):3350–5.

    CAS  PubMed  Google Scholar 

  73. Haase M, Bellomo R, Baldwin I, Haase-Fielitz A, Fealy N, Davenport P, et al. Hemodialysis membrane with a high-molecular-weight cutoff and cytokine levels in sepsis complicated by acute renal failure: a phase 1 randomized trial. Am J Kidney Dis. 2007;50(2):296–304.

    CAS  PubMed  Google Scholar 

  74. Wang J, Wu Z, Wen Q, Wang X. Effects of CRRT on renal function and toxin clearance in patients with sepsis: a case–control study. J Int Med Res. 2021;49(9):3000605211042981.

    CAS  PubMed  Google Scholar 

  75. Wang H-J, Wang P, Li N, Wan C, Jiang C-M, He J-S, et al. Effects of continuous renal replacement therapy on serum cytokines, neutrophil gelatinase-associated lipocalin, and prognosis in patients with severe acute kidney injury after cardiac surgery. Oncotarget. 2017;8(6):10628–36.

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  77. Shen J, Yu W, Chen Q, Shi J, Hu Y, Zhang 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.

    CAS  PubMed  Google Scholar 

  78. Mu TS, Palmer EG, Batts SG, Lentz-Kapua SL, Uyehara-Lock JH, Uyehara CFT. Continuous renal replacement therapy to reduce inflammation in a piglet hemorrhage–reperfusion extracorporeal membrane oxygenation model. Pediatr Res. 2012;72(3):249–55.

    CAS  PubMed  Google Scholar 

  79. Shi J, Chen Q, Yu W, Shen J, Gong J, He C, 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.

    CAS  PubMed  Google Scholar 

  80. McDonald CI, Fraser JF, Shekar K, Dunster KR, Thom O, Fung YL. Transfusion of packed red blood cells reduces selenium levels and increases lipid peroxidation in an in vivo ovine model. Transfus Med. 2014;24(1):50–4.

    CAS  PubMed  Google Scholar 

  81. Rich RR, Chaplin DD. Chapter 1—The human immune response. In: Rich RR, Fleisher TA, Shearer WT, Schroeder HW, Frew AJ, Weyand CM, editors. Clinical immunology. 5th ed. London: Content Repository Only; 2019. p. 3–17.e1.

    Google Scholar 

  82. Wang Y, Gao H, Shi C, Erhardt PW, Pavlovsky A, Soloviev DA, et al. Leukocyte integrin Mac-1 regulates thrombosis via interaction with platelet GPIbα. Nat Commun. 2017;8:15559.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Laurance S, Bertin F-R, Ebrahimian T, Kassim Y, Rys RN, Lehoux S, et al. Gas6 promotes inflammatory (CCR2 hi CX3CR1 lo) monocyte recruitment in venous thrombosis. Arterioscler Thromb Vasc Biol. 2017;37(7):1315–22.

    CAS  PubMed  Google Scholar 

  84. von Brühl M-L, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med. 2012;209(4):819–35.

    Google Scholar 

  85. Liu X, Xue Y, Ding T, Sun J. Enhancement of proinflammatory and procoagulant responses to silica particles by monocyte-endothelial cell interactions. Part Fibre Toxicol. 2012;9(1):36.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Michelson AD, Barnard MR, Krueger LA, Valeri CR, Furman MI. Circulating monocyte-platelet aggregates are a more sensitive marker of in vivo platelet activation than platelet surface P-selectin: studies in baboons, human coronary intervention, and human acute myocardial infarction. Circulation. 2001;104(13):1533–7.

    CAS  PubMed  Google Scholar 

  87. Li W, Ai X, Ni Y, Ye Z, Liang Z. The association between the neutrophil-to-lymphocyte ratio and mortality in patients with acute respiratory distress syndrome: a retrospective cohort study. Shock. 2019;51(2):161–7.

    PubMed  Google Scholar 

  88. Peng Y, Wang J, Xiang H, Weng Y, Rong F, Xue Y, et al. Prognostic value of neutrophil-lymphocyte ratio in cardiogenic shock: a cohort study. Med Sci Mon Int Med J Exp Clin Res. 2020;26:e922167.

    Google Scholar 

  89. Conway Morris A, Datta D, Shankar-Hari M, Stephen J, Weir CJ, Rennie J, et al. Cell-surface signatures of immune dysfunction risk-stratify critically ill patients: INFECT study. Intensive Care Med. 2018;44(5):627–35.

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Allen ML, Peters MJ, Goldman A, Elliott M, James I, Callard R, et al. Early postoperative monocyte deactivation predicts systemic inflammation and prolonged stay in pediatric cardiac intensive care. Crit Care Med. 2002;30(5):1140–5.

    PubMed  Google Scholar 

  91. Pfortmueller CA, Meisel C, Fux M, Schefold JC. Assessment of immune organ dysfunction in critical illness: utility of innate immune response markers. Intensive Care Med Exp. 2017;5(1):49.

    PubMed  PubMed Central  Google Scholar 

  92. Conway Morris A, Anderson N, Brittan M, Wilkinson TS, McAuley DF, Antonelli J, et al. Combined dysfunctions of immune cells predict nosocomial infection in critically ill patients. Br J Anaesth. 2013;111(5):778–87.

    CAS  PubMed  Google Scholar 

  93. Craddock PR, Fehr J, Dalmasso AP, Brighan KL, Jacob HS, Hemodialysis leukopenia. Pulmonary vascular leukostasis resulting from complement activation by dialyzer cellophane membranes. J Clin Invest. 1977;59(5):879–88.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Gral T, Schroth P, De Palma JR, Gordon A. Leukocyte dynamics with three types of hemodialyzers. Trans Am Soc Artif Intern Organs. 1969;15:45–9.

    CAS  PubMed  Google Scholar 

  95. Arnaout MA, Hakim RM, Todd RF 3rd, Dana N, Colten HR. Increased expression of an adhesion-promoting surface glycoprotein in the granulocytopenia of hemodialysis. N Engl J Med. 1985;312(8):457–62.

    CAS  PubMed  Google Scholar 

  96. Liakopoulos V, Jeron A, Shah A, Bruder D, Mertens PR, Gorny X. Hemodialysis-related changes in phenotypical features of monocytes. Sci Rep. 2018;8(1):13964.

    PubMed  PubMed Central  Google Scholar 

  97. 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.

    CAS  PubMed  Google Scholar 

  98. Zach TL, Steinhorn RH, Georgieff MK, Mills MM, Green TP. Leukopenia associated with extracorporeal membrane oxygenation in newborn infants. J Pediatr. 1990;116(3):440–4.

    CAS  PubMed  Google Scholar 

  99. Liu CH, Kuo SW, Ko WJ, Tsai PR, Wu SW, Lai CH, et al. Early measurement of IL-10 predicts the outcomes of patients with acute respiratory distress syndrome receiving extracorporeal membrane oxygenation. Sci Rep. 2017;7(1):1021.

    PubMed  PubMed Central  Google Scholar 

  100. Bredthauer A, Wilm J, Philipp A, Foltan M, Mueller T, Lehle K. The oxygenator design might influence the adhesion of leukocytes and deposits of von willebrand fibers on the surface of gas exchange membranes during ECMO. Eur J Heart Fail. 2017;19(S2):36–7.

    Google Scholar 

  101. Nockher WA, Wiemer J, Scherberich JE. Haemodialysis monocytopenia: differential sequestration kinetics of CD14+CD16+ and CD14++ blood monocyte subsets. Clin Exp Immunol. 2001;123(1):49–55.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  104. Skogby M, Mellgren K, Adrian K, Friberg LG, Chevalier JY, Mellgren G. Induced cell trauma during in vitro perfusion: a comparison between two different perfusion systems. Artif Organs. 1998;22(12):1045–51.

    CAS  PubMed  Google Scholar 

  105. Sirolli V, Ballone E, Di Stante S, Amoroso L, Bonomini M. Cell activation and cellular-cellular interactions during hemodialysis: effect of dialyzer membrane. Int J Artif Organs. 2002;25(6):529–37.

    CAS  PubMed  Google Scholar 

  106. Kaupke CJ, Zhang J, Cesario T, Yousefi S, Akeel N, Vaziri ND. Effect of hemodialysis on leukocyte adhesion receptor expression. Am J Kidney Dis. 1996;27(2):244–52.

    CAS  PubMed  Google Scholar 

  107. Rudensky B, Yinnon AM, Shutin O, Broide E, Wiener-Well Y, Bitran D, et al. The cellular immunological responses of patients undergoing coronary artery bypass grafting compared with those of patients undergoing valve replacement. Eur J Cardiothorac Surg. 2010;37(5):1056–62.

    PubMed  Google Scholar 

  108. Asimakopoulos G, Kohn A, Stefanou DC, Haskard DO, Landis RC, Taylor KM. Leukocyte integrin expression in patients undergoing cardiopulmonary bypass. Ann Thorac Surg. 2000;69(4):1192–7.

    CAS  PubMed  Google Scholar 

  109. Shimamura S, Kimura K, Katayama M, Mashita T, Maeda K, Kobayashi S, et al. Evaluation of neutrophil function during hemodialysis treatment in healthy dogs under anesthesia with sevoflurane. J Vet Med Sci. 2014;76(11):1539–43.

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Schnoor M, Parkos CA. Disassembly of endothelial and epithelial junctions during leukocyte transmigration. Front Biosci. 2008;13:6638–52.

    CAS  PubMed  Google Scholar 

  111. Rao AM, Apoorva R, Anand U, Anand CV, Venu G. Effect of Hemodialysis on plasma myeloperoxidase activity in end stage renal disease patients. Indian J Clin Biochem. 2012;27(3):253–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Ono K, Ueki K, Inose K, Tsuchida A, Yano S, Nojima Y. Plasma levels of myeloperoxidase and elastase are differentially regulated by hemodialysis membranes and anticoagulants. Res Commun Mol Pathol Pharmacol. 2000;108(5–6):341–9.

    CAS  PubMed  Google Scholar 

  113. Pham CT. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol. 2006;6(7):541–50.

    CAS  PubMed  Google Scholar 

  114. Lewis SL, Van Epps DE, Chenoweth DE. Leukocyte C5a receptor modulation during hemodialysis. Kidney Int. 1987;31(1):112–20.

    CAS  PubMed  Google Scholar 

  115. Verma SK, Molitoris BA. Renal endothelial injury and microvascular dysfunction in acute kidney injury. Semin Nephrol. 2015;35(1):96–107.

    CAS  PubMed  Google Scholar 

  116. Delano MJ, Ward PA. Sepsis-induced immune dysfunction: can immune therapies reduce mortality? J Clin Invest. 2016;126(1):23–31.

    PubMed  PubMed Central  Google Scholar 

  117. Corley A, Lye I, Lavana J, Ahuja A, Jarrett P, Anstey C, et al. Nosocomial infection rates in patients receiving extracorporeal membrane oxygenation across Australia and New Zealand: an interim analysis. Aust Crit Care. 2019;32:S12.

    Google Scholar 

  118. Mailloux LU, Bellucci AG, Wilkes BM, Napolitano B, Mossey RT, Lesser M, et al. Mortality in dialysis patients: analysis of the causes of death. Am J Kidney Dis. 1991;18(3):326–35.

    CAS  PubMed  Google Scholar 

  119. Sarnak MJ, Jaber BL. Mortality caused by sepsis in patients with end-stage renal disease compared with the general population. Kidney Int. 2000;58(4):1758–64.

    CAS  PubMed  Google Scholar 

  120. Lewis SL, Van Epps DE. Neutrophil and monocyte alterations in chronic dialysis patients. Am J Kidney Dis. 1987;9(5):381–95.

    CAS  PubMed  Google Scholar 

  121. Kawahito K, Kobayashi E, Misawa Y, Adachi H, Fujimura A, Ino T, et al. Recovery from lymphocytopenia and prognosis after adult extracorporeal membrane oxygenation. Arch Surg. 1998;133(2):216–7.

    CAS  PubMed  Google Scholar 

  122. Hong TH, Hu FC, Kuo SW, Ko WJ, Chow LP, Hsu LM, et al. Predicting outcome in patients under extracorporeal membrane oxygenation due to cardiogenic shock through dynamic change of lymphocytes and interleukins. IJC Metab Endocr. 2015;7:36–44.

    Google Scholar 

  123. DePalma L, Short BL, Meurs KV, Luban NLC. A flow cytometric analysis of lymphocyte subpopulations in neonates undergoing extracorporeal membrane oxygenation. J Pediatr. 1991;118(1):117–20.

    CAS  PubMed  Google Scholar 

  124. Sargin M, Mete MT, Erdogan SB, Kuplay H, Bastopcu M, Akansel S, et al. Prognostic value of neutrophil lymphocyte ratio for early renal failure in ECMO patients. J Heart Lung Transplant. 2019;38(4):S175.

    Google Scholar 

  125. Catabay C, Obi Y, Streja E, Soohoo M, Park C, Rhee CM, et al. Lymphocyte cell ratios and mortality among incident hemodialysis patients. Am J Nephrol. 2017;46(5):408–16.

    CAS  PubMed  Google Scholar 

  126. Zhao W-M, Tao S-M, Liu G-L. Neutrophil-to-lymphocyte ratio in relation to the risk of all-cause mortality and cardiovascular events in patients with chronic kidney disease: a systematic review and meta-analysis. Ren Fail. 2020;42(1):1059–66.

    PubMed  PubMed Central  Google Scholar 

  127. Lisowska KA, Dębska-Ślizień A, Jasiulewicz A, Heleniak Z, Bryl E, Witkowski JM. Hemodialysis affects phenotype and proliferation of CD4-positive T lymphocytes. J Clin Immunol. 2012;32(1):189–200.

    CAS  PubMed  Google Scholar 

  128. Ortega SB, Pandiyan P, Windsor J, Torres VO, Selvaraj UM, Lee A, et al. A pilot study identifying brain-targeting adaptive immunity in pediatric extracorporeal membrane oxygenation patients with acquired brain injury. Crit Care Med. 2019;47(3):e206–13.

    PubMed  PubMed Central  Google Scholar 

  129. Byrnes J, McKamie W, Swearingen C, Prodhan P, Bhutta A, Jaquiss R, et al. Hemolysis during cardiac extracorporeal membrane oxygenation: a case-control comparison of roller pumps and centrifugal pumps in a pediatric population. ASAIO J. 2011;57(5):456–61.

    PubMed  Google Scholar 

  130. 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.

    CAS  PubMed  Google Scholar 

  131. Mlejnsky F, Klein AA, Lindner J, Maruna P, Kvasnicka J, Kvasnicka T, et al. A randomised controlled trial of roller versus centrifugal cardiopulmonary bypass pumps in patients undergoing pulmonary endarterectomy. Perfusion. 2014;30(7):520–8.

    PubMed  Google Scholar 

  132. Perttilä J, Salo M, Peltola O. Comparison of the effects of centrifugal versus roller pump on the immune response in open-heart surgery. Perfusion. 1995;10(4):249–56.

    PubMed  Google Scholar 

  133. Baufreton C, Intrator L, Jansen PG, te Velthuis H, Le Besnerais P, Vonk A, et al. Inflammatory response to cardiopulmonary bypass using roller or centrifugal pumps. Ann Thorac Surg. 1999;67(4):972–7.

    CAS  PubMed  Google Scholar 

  134. Passaroni AC, Felicio ML, de Campos NLKL, de Moraes Silva MA, Yoshida WB. Hemolysis and inflammatory response to extracorporeal circulation during on-pump CABG: comparison between roller and centrifugal pump systems. Braz J Cardiovasc Surg. 2018;33(1):64–71.

    PubMed  PubMed Central  Google Scholar 

  135. Papadimas E, Leow L, Tan YK, Shen L, Ramanathan K, Choong AMTL, et al. Centrifugal and roller pumps in neonatal and pediatric extracorporeal membrane oxygenation: a systematic review and meta-analysis of clinical outcomes. ASAIO J. 2022;68(3):311–7.

    PubMed  Google Scholar 

  136. Halaweish I, Cole A, Cooley E, Lynch WR, Haft JW. Roller and centrifugal pumps: a retrospective comparison of bleeding complications in extracorporeal membrane oxygenation. ASAIO J. 2015;61(5):496–501.

    CAS  PubMed  Google Scholar 

  137. Ronco C, Clark WR. Haemodialysis membranes. Nat Rev Nephrol. 2018;14(6):394–410.

    CAS  PubMed  Google Scholar 

  138. Falkenhagen D, Bosch T, Brown GS, Schmidt B, Holtz M, Baurmeister U, et al. A clinical study on different cellulosic dialysis membranes. Nephrol Dial Transplant. 1987;2(6):537–45.

    CAS  PubMed  Google Scholar 

  139. Pereira BJ, King AJ, Poutsiaka DD, Strom JA, Dinarello CA. Comparison of first use and reuse of cuprophan membranes on interleukin-1 receptor antagonist and interleukin-1 beta production by blood mononuclear cells. Am J Kidney Dis. 1993;22(2):288–95.

    CAS  PubMed  Google Scholar 

  140. Hernandez MR, Palomo M, Fuste B, Carbó C, Collado S, Cases A, et al. Effect of two different dialysis membranes on leukocyte adhesion and aggregation. Nephron Clin Pract. 2007;106(1):c1–8.

    CAS  PubMed  Google Scholar 

  141. Cases A, Reverter JC, Escolar G, Sanz C, Lopez-Pedret J, Revert L, et al. Platelet activation on hemodialysis: influence of dialysis membranes. Kidney Int Suppl. 1993;41:S217–20.

    CAS  PubMed  Google Scholar 

  142. Hakim RM, Fearon DT, Lazarus JM, Perzanowski CS. Biocompatibility of dialysis membranes: effects of chronic complement activation. Kidney Int. 1984;26(2):194–200.

    CAS  PubMed  Google Scholar 

  143. Floris M, Marchionna N, Clementi A, Kim JC, Cruz DN, Nalesso F, et al. Evaluation of a new polysulfone hemofilter for continuous renal replacement therapy. Blood Purif. 2011;32(2):133–8.

    CAS  PubMed  Google Scholar 

  144. Yasuda H, Sekine K, Abe T, Suzaki S, Katsumi A, Harada N, et al. Comparison of two polysulfone membranes for continuous renal replacement therapy for sepsis: a prospective cross-over study. Ren Replace Ther. 2018;4(1):6.

    Google Scholar 

  145. Shibata M, Miyamoto K, Kato S. Comparison of the circulatory effects of continuous renal replacement therapy using AN69ST and polysulfone membranes in septic shock patients: a retrospective observational study. Ther Apher Dial. 2020;24(5):561–7.

    CAS  PubMed  Google Scholar 

  146. Ozturk S, Kazancioglu R, Sahin GM, Turkmen A, Gursu M, Sever MS. The effect of the type of membrane on intradialytic complications and mortality in crush syndrome. Ren Fail. 2009;31(8):655–61.

    CAS  PubMed  Google Scholar 

  147. Stahl RF, Fisher CA, Kucich U, Weinbaum G, Warsaw DS, Stenach N, et al. Effects of simulated extracorporeal circulation on human leukocyte elastase release, superoxide generation, and procoagulant activity. J Thorac Cardiovasc Surg. 1991;101(2):230–9.

    CAS  PubMed  Google Scholar 

  148. Bergman P, Belboul A, Friberg LG, 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.

    CAS  PubMed  Google Scholar 

  149. Wilm J, Philipp A, Muller T, Bredthauer A, Gleich O, Schmid C, et al. Leukocyte adhesion as an indicator of oxygenator thrombosis during extracorporeal membrane oxygenation therapy? ASAIO J. 2017;64(1):24–30.

    Google Scholar 

  150. Steiger T, Foltan M, Philipp A, Mueller T, Gruber M, Bredthauer A, et al. Accumulations of von Willebrand factor within ECMO oxygenators: potential indicator of coagulation abnormalities in critically ill patients? Artif Organs. 2019;43(11):1065–76.

    CAS  PubMed  PubMed Central  Google Scholar 

  151. Obstals F, Vorobii M, Riedel T, de Los Santos Pereira A, Bruns M, Singh S, et al. Improving hemocompatibility of membranes for extracorporeal membrane oxygenators by grafting nonthrombogenic polymer brushes. Macromol Biosci. 2018;18(3):1700359.

    Google Scholar 

  152. Kawahito S, Maeda T, Yoshikawa M, Takano T, Nonaka K, Linneweber J, et al. Blood trauma induced by clinically accepted oxygenators. ASAIO J. 2001;47(5):492–5.

    CAS  PubMed  Google Scholar 

  153. Meyer AD, Rishmawi AR, Kamucheka R, Lafleur C, Batchinsky AI, Mackman N, et al. Effect of blood flow on platelets, leukocytes, and extracellular vesicles in thrombosis of simulated neonatal extracorporeal circulation. J Thromb Haemost. 2020;18(2):399–410.

    CAS  PubMed  Google Scholar 

  154. Lehle K, Philipp A, Muller T, Schettler F, Bein T, Schmid C, et al. Flow dynamics of different adult ECMO systems: a clinical evaluation. Artif Organs. 2014;38(5):391–8.

    CAS  PubMed  Google Scholar 

  155. Sezai A, Shiono M, Nakata K-I, Hata M, Iida M, Saito A, et al. Effects of pulsatile CPB on interleukin-8 and endothelin-1 levels. Artif Organs. 2005;29(9):708–13.

    CAS  PubMed  Google Scholar 

  156. Watkins WD, Peterson MB, Kong DL, Kono K, Buckley MJ, Levine FH, et al. Thromboxane and prostacyclin changes during cardiopulmonary bypass with and without pulsatile flow. J Thorac Cardiovasc Surg. 1982;84(2):250–6.

    CAS  PubMed  Google Scholar 

  157. Watarida S, Mori A, Onoe M, Tabata R, Shiraishi S, Sugita T, et al. A clinical study on the effects of pulsatile cardiopulmonary bypass on the blood endotoxin levels. J Thorac Cardiovasc Surg. 1994;108(4):620–5.

    CAS  PubMed  Google Scholar 

  158. Onorati F, Santarpino G, Rubino AS, Caroleo S, Dardano A, Scalas C, et al. Body perfusion during adult cardiopulmonary bypass is improved by pulsatile flow with intra-aortic balloon pump. Int J Artif Organs. 2009;32(1):50–61.

    CAS  PubMed  Google Scholar 

  159. Li G, Zeng J, Liu Z, Zhang Y, Fan X. The pulsatile modification improves Hemodynamics and attenuates inflammatory responses in extracorporeal membrane oxygenation. J Inflamm Res. 2021;14:1357–64.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  161. Hall MW, Knatz NL, Vetterly C, Tomarello S, Wewers MD, Volk HD, et al. Immunoparalysis and nosocomial infection in children with multiple organ dysfunction syndrome. Intensive Care Med. 2011;37(3):525–32.

    CAS  PubMed  Google Scholar 

  162. Zheng H-Y, Zhang M, Yang C-X, Zhang N, Wang X-C, Yang X-P, et al. Elevated exhaustion levels and reduced functional diversity of T cells in peripheral blood may predict severe progression in COVID-19 patients. Cell Mol Immunol. 2020;17(5):541–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Bhat T, Teli S, Rijal J, Bhat H, Raza M, Khoueiry G, et al. Neutrophil to lymphocyte ratio and cardiovascular diseases: a review. Expert Rev Cardiovasc Ther. 2013;11(1):55–9.

    CAS  PubMed  Google Scholar 

  164. Tauber H, Streif W, Fritz J, Ott H, Weigel G, Loacker L, et al. Predicting transfusion requirements during extracorporeal membrane oxygenation. J Cardiothorac Vasc Anesth. 2016;30(3):692–701.

    PubMed  Google Scholar 

  165. Millar JE, Fanning JP, McDonald CI, McAuley DF, Fraser JF. The inflammatory response to extracorporeal membrane oxygenation (ECMO): a review of the pathophysiology. Crit Care. 2016;20(1):387.

    PubMed  PubMed Central  Google Scholar 

  166. Doyle AJ, Hunt BJ. Current understanding of how extracorporeal membrane oxygenators activate haemostasis and other blood components. Front Med. 2018;5:352.

    Google Scholar 

  167. Singh S. Anticoagulation during renal replacement therapy. Indian J Crit Care Med. 2020;24(Suppl 3):S112–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  168. Guidelines for adult respiratory failure (2013).

    Google Scholar 

  169. Stockmann H, Keller T, Büttner S, Jörres A, Kindgen-Milles D, Kunz JV, et al. CytoResc–“CytoSorb” rescue for critically ill patients undergoing the COVID-19 cytokine storm: a structured summary of a study protocol for a randomized controlled trial. Trials. 2020;21(1):577.

    CAS  PubMed  PubMed Central  Google Scholar 

  170. Iwata M, Suzuki S, Asai Y, Inoue T, Takagi K. Involvement of nitric oxide in a rat model of carrageenin-induced pleurisy. Mediat Inflamm. 2010;2010:682879.

    Google Scholar 

  171. Dal Secco D, Paron JA, de Oliveira SHP, Ferreira SH, Silva JS, de Queiroz Cunha F. Neutrophil migration in inflammation: nitric oxide inhibits rolling, adhesion and induces apoptosis. Nitric Oxide. 2003;9(3):153–64.

    CAS  PubMed  Google Scholar 

  172. Carreau A, Kieda C, Grillon C. Nitric oxide modulates the expression of endothelial cell adhesion molecules involved in angiogenesis and leukocyte recruitment. Exp Cell Res. 2011;317(1):29–41.

    CAS  PubMed  Google Scholar 

  173. James C, Millar J, Horton S, Brizard C, Molesworth C, Butt W. Nitric oxide administration during paediatric cardiopulmonary bypass: a randomised controlled trial. Intensive Care Med. 2016;42(11):1744–52.

    CAS  PubMed  Google Scholar 

  174. Checchia PA, Bronicki RA, Muenzer JT, Dixon D, Raithel S, Gandhi SK, et al. Nitric oxide delivery during cardiopulmonary bypass reduces postoperative morbidity in children—a randomized trial. J Thorac Cardiovasc Surg. 2013;146(3):530–6.

    CAS  PubMed  Google Scholar 

  175. Millar JE, Bartnikowski N, Passmore MR, Obonyo NG, Malfertheiner MV, von Bahr V, et al. Combined mesenchymal stromal cell therapy and ECMO in ARDS: a controlled experimental study in sheep. Am J Respir Crit Care Med. 2020;202(3):383–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  176. von Bahr V, Millar JE, Malfertheiner MV, Ki KK, Passmore MR, Bartnikowski N, et al. Mesenchymal stem cells may ameliorate inflammation in an ex vivo model of extracorporeal membrane oxygenation. Perfusion. 2019;34(1_suppl):15–21.

    Google Scholar 

  177. Zen K, Guo YL, Li LM, Bian Z, Zhang CY, Liu Y. Cleavage of the CD11b extracellular domain by the leukocyte serprocidins is critical for neutrophil detachment during chemotaxis. Blood. 2011;117(18):4885–94.

    PubMed  PubMed Central  Google Scholar 

  178. Harlan JM, Winn RK. Leukocyte-endothelial interactions: clinical trials of anti-adhesion therapy. Crit Care Med. 2002;30(5 Suppl):S214–9.

    CAS  PubMed  Google Scholar 

  179. Scholz M, Cinatl J, Barros RT, Lisboa AC, Genevcius CF, Margraf S, et al. First efficacy and safety results with the antibody containing leukocyte inhibition module in cardiac surgery patients with neutrophil hyperactivity. ASAIO J. 2005;51(2):144–7.

    CAS  PubMed  Google Scholar 

  180. Abdel-Rahman U, Margraf S, Aybek T, Lögters T, Bitu-Moreno J, Francischetti I, et al. Inhibition of neutrophil activity improves cardiac function after cardiopulmonary bypass. J Inflamm. 2007;4:21.

    Google Scholar 

  181. de Amorim CG, Malbouisson LMS, da Silva FC Jr, Fiorelli AI, Murakami CKF, Carmona MJC. Leukocyte depletion during CPB: effects on inflammation and lung function. Inflammation. 2014;37(1):196–204.

    CAS  PubMed  Google Scholar 

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Ki, K.K., Heinsar, S., Langguth, D., Fraser, J.F. (2023). Extracorporeal Circulation-Related Immune Response. In: Molnar, Z., Ostermann, M., Shankar-Hari, M. (eds) Management of Dysregulated Immune Response in the Critically Ill. Lessons from the ICU. Springer, Cham. https://doi.org/10.1007/978-3-031-17572-5_5

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