Consensus Statement: Defining Minimal Criteria for Reporting the Systemic Inflammatory Response to Cardiopulmonary Bypass
DOI:
https://doi.org/10.1532/HSF98Abstract
The causal factors of the systemic inflammatory response to cardiopulmonary bypass (CPB) were correctly identified in the early 1990s: "… activation of complement, coagulation, fibrinolytic, and kallikrein cascades, activation of neutrophils with degranulation and protease enzyme release, oxygen radical production, and the synthesis of various cytokines from mononuclear cells" [Butler 1993]. Why therefore have clinical advances to curb the systemic inflammatory response proven such a disappointment? Part of the problem is that cardiac surgery has never taken intellectual ownership of this issue, borrowing its diagnosis from critical care medicine and failing to define the minimal criteria that should be measured when reporting on the systemic inflammatory response. An evidence based review of the current literature by many of the coauthors on this paper found that the majority of studies on the systemic inflammatory response did not measure a single one of the causal factors listed above - thus hindering our ability to identify mechanisms of causation and identify drug targets [Landis 2008]. A panel of experts convened at the Outcomes XII meeting, Barbados 2008, drafted the present consensus document in order to provide a framework to guide future studies and interdictions of the systemic inflammatory response. Herein, we have recommended: 1) mandatory reporting of minimal CPB and perfusion criteria that may affect outcomes, 2) reporting of a minimal set of causal inflammatory markers linked to adverse sequelae, and 3) reporting of at least one clinical end-point of organ injury, from a list of endpoints and markers of organ injury that balance practicality with clinical meaningfulness. It is our collective belief that this document will serve as a foundation for furthering our understanding of the influence of CPB practice with the systemic inflammatory response by standardizing the reporting of research findings in the peer-reviewed literature.References
Aldea GS, Soltow LO, Chandler WL, Triggs CM, Vocelka CR, Crockett GI, Shin YT, Curtis WE, Verrier ED. 2002. Limitation of thrombin generation, platelet activation, and inflammation by elimination of cardiotomy suction in patients undergoing coronary artery bypass grafting treated with heparinbonded circuits. J Thorac. Cardiovasc. Surg 123:742-55.nAllen S, McBride WT, Young IS, MacGowan SW, McMurray TJ, Prabhu S, Penugonda SP, Armstrong MA. 2005. A clinical, renal and immunological assessment of surface modifying additive treated (SMART) cardiopulmonary bypass circuits. Perfusion 20:255-62.nAllen SJ, McBride WT, McMurray TJ, Phillips AS, Penugonda SP, Campalani G, Young IS, Armstrong MA. 2007. Cell salvage alters the systemic inflammatory response after off-pump coronary artery bypass grafting surgery. Ann. Thorac. Surg 83:578-85.nAnttila V, Hagino I, Iwata I, Mettler BA, Lidov HG, Zurakowski D, Jonas RA. 2006. Aprotinin improves cerebral protection: evidence from a survival porcine model. J Thorac. Cardiovasc. Surg 132:948-53.nBanbury MK, Brizzio ME, Rajeswaran J, Lytle BW, Blackstone EH. 2006. Transfusion increases the risk of postoperative infection after cardiovascular surgery. J Am. Coll. Surg 202:131-8.nBone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RM, Sibbald WJ. 1992. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 101:1644-55.nBrown MC, Donnelly JE. 2000. Impact of closed versus open venous reservoirs on patient outcomes in isolated coronary artery bypass graft surgery. Perfusion 15:467-72.nBrown WR, Moody DM, Challa VR, Stump DA, Hammon JW. 2000. Longer duration of cardiopulmonary bypass is associated with greater numbers of cerebral microemboli. Stroke 31:707-13.nBurris NS, Brown EN, Grant M, Kon ZN, Gibber M, Gu J, Schwartz K, Kallam S, Joshi A, Vitali R, Poston RS. 2008. Optical coherence tomography imaging as a quality assurance tool for evaluating endoscopic harvest of the radial artery. Ann. Thorac. Surg 85:1271-7.nButler J, Rocker GM, Westaby S. 1993. Inflammatory response to cardiopulmonary bypass. Ann. Thorac. Surg 55:552-9.nChristen S, Finckh B, Lykkesfeldt J, Gessler P, Frese-Schaper M, Nielsen P, Schmid ER, Schmitt B. 2005. Oxidative stress precedes peak systemic inflammatory response in pediatric patients undergoing cardiopulmonary bypass operation. Free Radic. Biol. Med. 38:1323-32.nClark WM, Madden KP, Rothlein R, Zivin JA. 1991. Reduction of central nervous system ischemic injury in rabbits using leukocyte adhesion antibody treatment. Stroke 22:877-83.nCribbs SK, Martin GS, Rojas M. 2008. Monitoring of endothelial dysfunction in critically ill patients: the role of endothelial progenitor cells. Curr. Opin. Crit Care 14:354-60.nDavis CL, Kausz AT, Zager RA, Kharasch ED, Cochran RP. 1999. Acute renal failure after cardiopulmonary bypass in related to decreased serum ferritin levels. J Am. Soc. Nephrol. 10:2396-402.nDe Hert SG, Turani F, Mathur S, Stowe DF. 2005. Cardioprotection with volatile anesthetics: mechanisms and clinical implications. Anesth. Analg. 100:1584-93.nDe Somer F, Van BY, Caes F, Francois K, Arnout J, Bossuyt X, Taeymans Y, Van NG. 2002. Phosphorylcholine coating offers natural platelet preservation during cardiopulmonary bypass. Perfusion 17:39-44.nDiego RP, Mihalakakos PJ, Hexum TD, Hill GE. 1997. Methylprednisolone and full-dose aprotinin reduce reperfusion injury after cardiopulmonary bypass. J. Cardiothorac. Vasc. Anesth. 11:29-31.nEntman ML, Youker K, Shoji T, Kukielka G, Shappell SB, Taylor AA, Smith CW. 1992. Neutrophil induced oxidative injury of cardiac myocytes. A compartmented system requiring CD11b/CD18-ICAM-1 adherence. J Clin. Invest 90:1335-45.nEppinger MJ, Jones ML, Deeb GM, Bolling SF, Ward PA. 1995. Pattern of injury and the role of neutrophils in reperfusion injury of rat lung. J Surg Res. 58:713-18.nEvans BJ, Haskard DO, Finch JR, Hambleton IR, Landis RC, Taylor KM. 2008. The inflammatory effect of cardiopulmonary bypass on leukocyte extravasation in vivo. J Thorac. Cardiovasc. Surg 135: 999-1006.nFurnary AP, Wu Y, Hiratzka LF, Grunkemeier GL, Page US, III. 2007. Aprotinin does not increase the risk of renal failure in cardiac surgery patients. Circulation 116:I127-33.nGiomarelli P, Scolletta S, Borrelli E, Biagioli B. 2003. Myocardial and lung injury after cardiopulmonary bypass: role of interleukin (IL)-10. Ann. Thorac. Surg 76:117-23.nGoudeau JJ, Clermont G, Guillery O, Lemaire-Ewing S, Musat A, Vernet M, Vergely C, Guiguet M, Rochette L, Girard C. 2007. In high-risk patients, combination of antiinflammatory procedures during cardiopulmonary bypass can reduce incidences of inflammation and oxidative stress. J Cardiovasc. Pharmacol. 49:39-45.nHabib RH, Zacharias A, Schwann TA, Riordan CJ, Engoren M, Durham SJ, Shah A. 2005. Role of hemodilutional anemia and transfusion during cardiopulmonary bypass in renal injury after coronary revascularization: implications on operative outcome. Crit Care Med. 33:1749-56.nHammon JW, Stump DA, Butterworth JF, Moody DM, Rorie K, Deal DD, Kincaid EH, Oaks TE, KonND. 2006. Single crossclamp improves 6-month cognitive outcome in high-risk coronary bypass patients: the effect of reduced aortic manipulation. J Thorac. Cardiovasc. Surg 131:114-21.nHaugen O, Farstad M, Myklebust R, Kvalheim V, Hammersborg S, Husby P. 2007. Low perfusion pressure during CPB may induce cerebral metabolic and ultrastructural changes. Scand. Cardiovasc. J 41:331-8.nHill GE, Pohorecki R, Alonso A, Rennard SI, Robbins RA. 1996. Aprotinin reduces interleukin-8 production and lung neutrophil accumulation after cardiopulmonary bypass. Anesth. Analg. 83:696-700.nHsu LL, Champion HC, Campbell-Lee SA, Bivalacqua TJ, Manci EA, Diwan BA, Schimel DM, Cochard AE, Wang X, Schechter AN, Noguchi CT, Gladwin MT. 2007. Hemolysis in sickle cell mice causes pulmonary hypertension due to global impairment in nitric oxide bioavailability. Blood 109:3088-98.nJones TJ, Deal DD, Vernon JC, Blackburn N, Stump DA. 2002a. Does vacuum-assisted venous drainage increase gaseous microemboli during cardiopulmonary bypass? Ann. Thorac. Surg 74:2132-7.nJones TJ, Deal DD, Vernon JC, Blackburn N, Stump DA. 2002b. How effective are cardiopulmonary bypass circuits at removing gaseous microemboli? J Extra. Corpor. Technol. 34:34-9.nKamiya T, Katayama Y, Kashiwagi F, Terashi A. 1993. The role of bradykinin in mediating ischemic brain edema in rats. Stroke 24:571-5.nKaplanski G, Marin V, Fabrigoule M, Boulay V, Benoliel AM, Bongrand P, Kaplanski S, Farnarier C. 1998. Thrombin-activated human endothelial cells support monocyte adhesion in vitro following expression of intercellular adhesion molecule-1 (ICAM-1; CD54) and vascular cell adhesion molecule-1 (VCAM-1; CD106). Blood 92:1259-67.nKat GJ, McGowan V, Machado RF, Little JA, Taylor J, Morris CR, Nichols JS, Wang X, Poljakovic M, Morris SM, Jr., Gladwin MT. 2006. Lactate dehydrogenase as a biomarker of hemolysis-associated nitric oxide resistance, priapism, leg ulceration, pulmonary hypertension, and death in patients with sickle cell disease. Blood 107:2279-85.nKincaid EH, Ashburn DA, Hoyle JR, Reichert MG, Hammon JW, Kon ND. 2005. Does the combination of aprotinin and angiotensin-converting enzyme inhibitor cause renal failure after cardiac surgery? Ann. Thorac. Surg. 80:1388-93.nLandis C. 2007. Pharmacologic strategies for combating the inflammatory response. J Extra. Corpor. Technol. 39:291-5.nLandis C. 2007. Why the inflammatory response is important to the cardiac surgical patient. J Extra. Corpor. Technol. 39, 281-284.nLandis RC, Brown JR, Murkin JM, Likosky DS, Baker RA. 2008. An evidence-based review of pharmaceutical interventions to limit the systemic inflammatory response in cardiac surgery. Heart Surg.Forum in press.nLevy JH. 2008. Pharmacologic methods to reduce perioperative bleeding. Transfusion 48:31S-8S.nLidington EA, Haskard DO, Mason JC. 2000. Induction of decay-accelerating factor by thrombin through a protease-activated receptor 1 and protein kinase C-dependent pathway protects vascular endothelial cells from complement-mediated injury. Blood 96:2784-92.nMalik I, Danesh J, Whincup P, Bhatia V, Papacosta O, Walker M, Lennon L, Thomson A, Haskard D. 2001. Soluble adhesion molecules and prediction of coronary heart disease: a prospective study and meta-analysis. Lancet 358:971-6.nMcBride WT, Armstrong MA, Crockard AD, McMurray TJ, Rea JM. 1995. Cytokine balance and immunosuppressive changes at cardiac surgery: contrasting response between patients and isolated CPB circuits. Br. J Anaesth. 75:724-33.nMinneci PC, Deans KJ, Zhi H, Yuen PS, Star RA, Banks SM, Schechter AN, Natanson C, Gladwin MT, Solomon SB. 2005. Hemolysis-associated endothelial dysfunction mediated by accelerated NO inactivation by decompartmentalized oxyhemoglobin. J Clin. Invest 115:3409-17.nMurkin JM, Adams SJ, Novick RJ, Quantz M, Bainbridge D, Iglesias I, Cleland A, Schaefer B, Irwin B, Fox S. 2007. Monitoring brain oxygen saturation during coronary bypass surgery: a randomized, prospective study. Anesth. Analg. 104L51-8.nPoston RS, Gu J, Brown JM, Gammie JS, White C, Nie L, Pierson RN, III, Griffith BP. 2006. Endothelial injury and acquired aspirin resistance as promoters of regional thrombin formation and early vein graft failure after coronary artery bypass grafting. J Thorac. Cardiovasc. Surg 131:122-30.nRabelink TJ, de Boer HC, de Koning EJ, van Zonneveld AJ. 2004. Endothelial progenitor cells: more than an inflammatory response? Arterioscler. Thromb. Vasc. Biol. 24:834-8.nRadaelli A, Loardi C, Cazzaniga M, Balestri G, DeCarlini C, Cerrito MG, Cusa EN, Guerra L, Garducci S, Santo D, Menicanti L, Paolini G, Azzellino A, Lavitrano ML, Mancia G, Ferrari AU. 2007. Inflammatory activation during coronary artery surgery and its dose-dependent modulation by statin/ACE-inhibitor combination. Arterioscler. Thromb. Vasc. Biol. 27:2750-5.nRanucci M, Isgro G, Romitti F, Mele S, Biagioli B, Giomarelli P. 2006. Anaerobic metabolism during cardiopulmonary bypass: predictive value of carbon dioxide derived parameters. Ann. Thorac. Surg 81:2189-95.nRanucci M, Romitti F, Isgro G, Cotza M, Brozzi S, Boncilli A, Ditta A. 2005. Oxygen delivery during cardiopulmonary bypass and acute renal failure after coronary operations. Ann. Thorac. Surg 80:2213-20.nRinder CS, Rinder HM, Johnson K, Smith M, Lee DL, Tracey J, Polack G, Higgins P, Yeh CG, Smith BR. 1999. Role of C3 cleavage in monocyte activation during extracorporeal circulation. Circulation 100:553-8.nRinder CS, Smith MJ, Rinder HM, Cortright DN, Brodbeck RM, Krause JE, Smith BR. 2007. Leukocyte effects of C5a-receptor blockade during simulated extracorporeal circulation. Ann. Thorac. Surg 83:146-52.nRothlein R, Kishimoto TK, Mainolfi E. 1994. Cross-linking of ICAM-1 induces co-signaling of an oxidative burst from mononuclear leukocytes. J Immunol. 152:2488-95.nRubens FD, Nathan H, Labow R, Williams KS, Wozny D, Karsh J, Ruel M, Mesana T. 2005. Effects of methylprednisolone and a biocompatible copolymer circuit on blood activation during cardiopulmonary bypass. Ann. Thorac. Surg 79:655-65.nScheubel RJ, Zorn H, Silber RE, Kuss O, Morawietz H, Holtz J, Simm A. 2003. Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J Am. Coll. Cardiol. 42:2073-80.nSchwartz AE, Sandhu AA, Kaplon RJ, Young WL, Jonassen AE, Adams DC, Edwards NM, Sistino JJ, Kwiatkowski P, Michler RE. 1995. Cerebral blood flow is determined by arterial pressure and not cardiopulmonary bypass flow rate. Ann. Thorac. Surg 60:165-9.nSeekamp A, Mulligan MS, Till GO, Smith CW, Miyasaka M, Tamatani T, Todd RF, III, Ward PA. 1993. Role of beta 2 integrins and ICAM-1 in lung injury following ischemia-reperfusion of rat hind limbs. Am. J Pathol. 143:464-72.nShann KG, Likosky DS, Murkin JM, Baker RA, Baribeau YR, DeFoe GR, Dickinson TA, Gardner TJ, Grocott HP, O'Connor GT, Rosinski DJ, Sellke FW, Willcox TW. 2006. An evidence-based review of the practice of cardiopulmonary bypass in adults: a focus on neurologic injury, glycemic control, hemodilution, and the inflammatory response. J. Thorac. Cardiovasc. Surg. 132:283-90.nShappell SB, Toman C, Anderson DC, Taylor AA, Entman ML, Smith CW. 1990. Mac-1 (CD11b/CD18) mediates adherence-dependent hydrogen peroxide production by human and canine neutrophils. J Immunol. 144:2702-11.nShigeta O, Kojima H, Jikuya T, Terada Y, Atsumi N, Sakakibara Y, Nagasawa T, Mitsui T. 1997. Aprotinin inhibits plasmin-induced platelet activation during cardiopulmonary bypass. Circulation 96:569-74.nSpiess BD, Royston D, Levy JH, Fitch J, Dietrich W, Body S, Murkin J, Nadel A. 2004. Platelet transfusions during coronary artery bypass graft surgery are associated with serious adverse outcomes. Transfusion 44:1143-8.nStensrud PE, Nuttall GA, de Castro MA, Abel MD, Ereth MH, Oliver WC, Jr, Bryant SC, Schaff HV. 1999. A prospective, randomized study of cardiopulmonary bypass temperature and blood transfusion. Ann. Thorac. Surg 67:711-5.nStump DA. 2007. Deformable emboli and inflammation: temporary or permanent damage? J Extra. Corpor. Technol. 39:289-90.nSyrovets T, Tippler B, Rieks M, Simmet T. 1997. Plasmin is a potent and specific chemoattractant for human peripheral monocytes acting via a cyclic guanosine monophosphate-dependent pathway. Blood 89:4574-83.nTanaka K, Kanamori Y, Sato T, Kondo C, Katayama Y, Yada I, Yuasa H, Kusagawa M. 1991. Administration of haptoglobin during cardiopulmonary bypass surgery. ASAIO Trans. 37:M482-3.nTaylor KM. 1998. Central nervous system effects of cardiopulmonary bypass. Ann. Thorac. Surg. 66:S20-4.nTousoulis D, Andreou I, Antoniades C, Tentolouris C, Stefanadis C. 2008. Role of inflammation and oxidative stress in endothelial progenitor cell function and mobilization: Therapeutic implications for cardiovascular diseases. Atherosclerosis.nVerrier ED, Shernan SK, Taylor KM, Van de WF, Newman MF, Chen JC, Carrier M, Haverich A, Malloy KJ, Adams PX, Todaro TG, Mojcik CF, Rollins SA, Levy JH. 2004. Terminal complement blockade with pexelizumab during coronary artery bypass graft surgery requiring cardiopulmonary bypass: a randomized trial. JAMA 291:2319-27.nWachtfogel YT, Kucich U, Hack CE, Gluszko P, Niewiarowski S, Colman RW, Edmunds LH, Jr. 1993. Aprotinin inhibits the contact, neutrophil, and platelet activation systems during simulated extracorporeal perfusion. J. Thorac. Cardiovasc. Surg. 106:1-9.nWeiss SJ. 1989. Tissue destruction by neutrophils. N. Engl. J Med. 320:365-76.nWojciak-Stothard B, Potempa S, Eichholtz T, Ridley AJ. 2001. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci. 114:1343-55.n
