Effect of nitric oxide on postoperative acute kidney injury in patients who underwent cardiopulmonary bypass: a systematic review and meta-analysis with trial sequential analysis
Tóm tắt
The effect of nitric oxide (NO) on renal function is controversial in critical illness. We performed a systematic meta-analysis and trial sequential analysis to determine the effect of NO gas on renal function and other clinical outcomes in patients requiring cardiopulmonary bypass (CPB). The primary outcome was the relative risk (RR) of acute kidney injury (AKI), irrespective of the AKI stage. The secondary outcome was the mean difference (MD) in the length of ICU and hospital stay, the RR of postoperative hemorrhage, and the MD in levels of methemoglobin. Trial sequential analysis (TSA) was performed for the primary outcome. 54 trials were assessed for eligibility and 5 studies (579 patients) were eligible for meta-analysis. NO was associated with reduced risk of AKI (RR 0.76, 95% confidential interval [CI], 0.62 to 0.93, I2 = 0%). In the subgroup analysis by NO initiation timing, NO did not decrease the risk of AKI when started at the end of CPB (RR 1.20, 95% CI 0.52–2.78, I2 = 0%). However, NO did significantly reduce the risk of AKI when started from the beginning of CPB (RR 0.71, 95% CI 0.54–0.94, I2 = 10%). We conducted TSA based on three trials (400 patients) using KDIGO criteria and with low risk of bias. TSA indicated a CI of 0.50–1.02 and an optimal information size of 589 patients, suggesting a lack of definitive conclusion. Furthermore, NO does not affect the length of ICU and hospital stay or the risk of postoperative hemorrhage. NO slightly increased the level of methemoglobin at the end of CPB (MD 0.52%, 95% CI 0.27–0.78%, I2 = 90%), but it was clinically negligible. NO appeared to reduce the risk of postoperative AKI in patients undergoing CPB. Additional studies are required to ascertain the finding and further determine the dosage, timing and duration of NO administration.
Tài liệu tham khảo
Billings FTT, Hendricks PA, Schildcrout JS, Shi Y, Petracek MR, Byrne JG, et al. High-dose perioperative atorvastatin and acute kidney injury following cardiac surgery: a randomized clinical trial. JAMA. 2016;315(9):877–88.
Zarbock A, Schmidt C, Van Aken H, Wempe C, Martens S, Zahn PK, et al. Effect of remote ischemic preconditioning on kidney injury among high-risk patients undergoing cardiac surgery: a randomized clinical trial. JAMA. 2015;313(21):2133–41.
Bove T, Zangrillo A, Guarracino F, Alvaro G, Persi B, Maglioni E, et al. Effect of fenoldopam on use of renal replacement therapy among patients with acute kidney injury after cardiac surgery: a randomized clinical trial. JAMA. 2014;312(21):2244–53.
Meersch M, Schmidt C, Hoffmeier A, Van Aken H, Wempe C, Gerss J, et al. Prevention of cardiac surgery-associated AKI by implementing the KDIGO guidelines in high risk patients identified by biomarkers: the PrevAKI randomized controlled trial. Intensive Care Med. 2017;43(11):1551–61.
Vermeulen Windsant IC, Hanssen SJ, Buurman WA, Jacobs MJ. Cardiovascular surgery and organ damage: time to reconsider the role of hemolysis. J Thorac Cardiovasc Surg. 2011;142(1):1–11.
Vermeulen Windsant IC, de Wit NC, Sertorio JT, van Bijnen AA, Ganushchak YM, Heijmans JH, et al. Hemolysis during cardiac surgery is associated with increased intravascular nitric oxide consumption and perioperative kidney and intestinal tissue damage. Front Physiol. 2014;5:340.
Wessel DL, Adatia I, Giglia TM, Thompson JE, Kulik TJ. Use of inhaled nitric oxide and acetylcholine in the evaluation of pulmonary hypertension and endothelial function after cardiopulmonary bypass. Circulation. 1993;88(5 Pt 1):2128–38.
Ahmad A, Dempsey SK, Daneva Z, Azam M, Li N, Li PL, et al. Role of nitric oxide in the cardiovascular and renal systems. Int J Mol Sci. 2018;19:9.
Nelin LD, Potenziano JL. Inhaled nitric oxide for neonates with persistent pulmonary hypertension of the newborn in the CINRGI study: time to treatment response. BMC Pediatr. 2019;19(1):17.
Hunt JL, Bronicki RA, Anas N. Role of inhaled nitric oxide in the management of severe acute respiratory distress syndrome. Front Pediatr. 2016;4:74.
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.
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.
Rajek A, Pernerstorfer T, Kastner J, Mares P, Grabenwoger M, Sessler DI, et al. Inhaled nitric oxide reduces pulmonary vascular resistance more than prostaglandin E(1) during heart transplantation. Anesth Analg. 2000;90(3):523–30.
Zhou HL, Zhang R, Anand P, Stomberski CT, Qian Z, Hausladen A, et al. Metabolic reprogramming by the S-nitroso-CoA reductase system protects against kidney injury. Nature. 2019;565(7737):96–100.
Ahmad A, Sattar MA, Rathore HA, Abdulla MH, Khan SA, Abdullah NA, et al. Enhanced expression of endothelial nitric oxide synthase in the myocardium ameliorates the progression of left ventricular hypertrophy in l-arginine treated Wistar-Kyoto rats. J Physiol Pharmacol. 2016;67(1):31–44.
Berra L, Pinciroli R, Stowell CP, Wang L, Yu B, Fernandez BO, et al. Autologous transfusion of stored red blood cells increases pulmonary artery pressure. Am J Respir Crit Care Med. 2014;190(7):800–7.
Minneci PC, Deans KJ, Zhi H, Yuen PS, Star RA, Banks SM, et al. Hemolysis-associated endothelial dysfunction mediated by accelerated NO inactivation by decompartmentalized oxyhemoglobin. J Clin Investig. 2005;115(12):3409–17.
Lei C, Berra L, Rezoagli E, Yu B, Dong H, Yu S, et al. Nitric oxide decreases acute kidney injury and stage 3 chronic kidney disease after cardiac surgery. Am J Respir Crit Care Med. 2018;198(10):1279–87.
Kamenshchikov N. Nitric oxide in CPB for renal protection in cardiac surgery (NephroNO). NCT03527381.
Ruan SY, Huang TM, Wu HY, Wu HD, Yu CJ, Lai MS. Inhaled nitric oxide therapy and risk of renal dysfunction: a systematic review and meta-analysis of randomized trials. Crit Care (London, England). 2015;19:137.
Fernandes JL, Sampaio RO, Brandao CM, Accorsi TA, Cardoso LF, Spina GS, et al. Comparison of inhaled nitric oxide versus oxygen on hemodynamics in patients with mitral stenosis and severe pulmonary hypertension after mitral valve surgery. Am J Cardiol. 2011;107(7):1040–5.
Potapov E, Meyer D, Swaminathan M, Ramsay M, El Banayosy A, Diehl C, et al. Inhaled nitric oxide after left ventricular assist device implantation: a prospective, randomized, double-blind, multicenter, placebo-controlled trial. J Heart Lung Transplant. 2011;30(8):870–8.
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ (Clinical research ed). 2009;339:b2535.
Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ (Clinical research ed). 2011;343:d5928.
Greco TBZG, Gemma M, et al. How to impute study-specific standard deviations in meta-analyses of skewed continuous endpoints? World J Meta-Anal. 2015;3:215–24.
Higgins JPT GSe. Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration. 2011. http://handbook.cochrane.org.
Jin ZC, Zhou XH, He J. Statistical methods for dealing with publication bias in meta-analysis. Stat Med. 2015;34(2):343–60.
Borenstein MHL, Higgins JPT, et al. Introduction to meta-analysis. Chichester: Wiley; 2009.
Bradburn MJ, Deeks JJ, Berlin JA, Russell Localio A. Much ado about nothing: a comparison of the performance of meta-analytical methods with rare events. Stat Med. 2007;26(1):53–77.
Wetterslev J, Jakobsen JC, Gluud C. Trial Sequential analysis in systematic reviews with meta-analysis. BMC Med Res Methodol. 2017;17(1):39.
Kamenshchikov NO, Mandel IA, Podoksenov YK, Svirko YS, Lomivorotov VV, Mikheev SL, et al. Nitric oxide provides myocardial protection when added to the cardiopulmonary bypass circuit during cardiac surgery: randomized trial. J Thorac Cardiovasc Surg. 2018;157:2328.
Perrin G, Roch A, Michelet P, Reynaud-Gaubert M, Thomas P, Doddoli C, et al. Inhaled nitric oxide does not prevent pulmonary edema after lung transplantation measured by lung water content: a randomized clinical study. Chest. 2006;129(4):1024–30.
Vercaemst L. Hemolysis in cardiac surgery patients undergoing cardiopulmonary bypass: a review in search of a treatment algorithm. J Extra Corpor Technol. 2008;40(4):257–67.
Rezoagli E, Ichinose F, Strelow S, Roy N, Shelton K, Matsumine R, et al. Pulmonary and systemic vascular resistances after cardiopulmonary bypass: role of hemolysis. J Cardiothorac Vasc Anesth. 2017;31(2):505–15.
Reiter CD, Wang X, Tanus-Santos JE, Hogg N, Cannon RO 3rd, Schechter AN, et al. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat Med. 2002;8(12):1383–9.
Rother RP, Bell L, Hillmen P, Gladwin MT. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. JAMA. 2005;293(13):1653–62.
Zadek F, Spina S, Hu J, Berra L. Recommended reading from the Massachusetts general hospital, department of anesthesia, critical care and pain medicine fellows. Am J Respir Crit Care Med. 2019;200:628–30.
Troncy E, Francoeur M, Salazkin I, Yang F, Charbonneau M, Leclerc G, et al. Extra-pulmonary effects of inhaled nitric oxide in swine with and without phenylephrine. Br J Anaesth. 1997;79(5):631–40.
Matsuo N. The role of intrapulmonary nitric oxide generation in the development of adult respiratory distress syndrome. Surg Today. 1999;29(10):1068–74.
Gozdzik W, Albert J, Harbut P, Zielinski S, Ryniak S, Lindwall R, et al. Prolonged exposure to inhaled nitric oxide transiently modifies tubular function in healthy piglets and promotes tubular apoptosis. Acta Physiol (Oxford, England). 2009;195(4):495–502.
Valvini EM, Young JD. Serum nitrogen oxides during nitric oxide inhalation. Br J Anaesth. 1995;74(3):338–9.
Liu C, Zhao W, Christ GJ, Gladwin MT, Kim-Shapiro DB. Nitric oxide scavenging by red cell microparticles. Free Radical Biol Med. 2013;65:1164–73.
Sundd P, Gladwin MT, Novelli EM. Pathophysiology of sickle cell disease. Ann Rev Pathol. 2019;14:263–92.
Young JD, Dyar O, Xiong L, Howell S. Methaemoglobin production in normal adults inhaling low concentrations of nitric oxide. Intensive Care Med. 1994;20(8):581–4.
Fattouch K, Sbraga F, Sampognaro R, Bianco G, Gucciardo M, Lavalle C, et al. Treatment of pulmonary hypertension in patients undergoing cardiac surgery with cardiopulmonary bypass: a randomized, prospective, double-blind study. J Cardiovasc Med (Hagerstown). 2006;7(2):119–23.
Kirbas A, Yalcin Y, Tanrikulu N, Gurer O, Isik O. Comparison of inhaled nitric oxide and aerosolized iloprost in pulmonary hypertension in children with congenital heart surgery. Cardiol J. 2012;19(4):387–94.
Knothe C, Scholz S, Zickmann B, Marquart B, Dapper F, Hempelmann G. NO inhalation in heart surgery procedures: relevance for right heart function? Der Anaesthesist. 1996;45(3):240–8.
Solina A, Papp D, Ginsberg S, Krause T, Grubb W, Scholz P, et al. A comparison of inhaled nitric oxide and milrinone for the treatment of pulmonary hypertension in adult cardiac surgery patients. J Cardiothorac Vasc Anesth. 2000;14(1):12–7.
Fattouch K, Sbraga F, Bianco G, Speziale G, Gucciardo M, Sampognaro R, et al. Inhaled prostacyclin, nitric oxide, and nitroprusside in pulmonary hypertension after mitral valve replacement. J Card Surg. 2005;20(2):171–6.
Prendergast B, Scott DH, Mankad PS. Beneficial effects of inhaled nitric oxide in hypoxaemic patients after coronary artery bypass surgery. Eur J Cardiothorac Surg. 1998;14(5):488–93.
Lei C, Berra L, Xiong L, Zapol WM. Reply to Coutrot et al.: is nitric oxide nephro- or cardioprotective? Am J Respir Crit Care Med. 2019;199(11):1442–3.
Sardo S, Osawa EA, Finco G, Gomes Galas FRB, de Almeida JP, Cutuli SL, et al. Nitric oxide in cardiac surgery: a meta-analysis of randomized controlled trials. J Cardiothorac Vasc Anesth. 2018;32(6):2512–9.
Irokawa M, Nishinaga M, Ikeda U, Shinoda Y, Suematsu M, Gouda N, et al. Endothelial-derived nitric oxide preserves anticoagulant heparan sulfate expression in cultured porcine aortic endothelial cells. Atherosclerosis. 1997;135(1):9–17.
Marcucci L. Avoiding common ICU errors. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins; 2007.
Bellomo R, Ronco C, Kellum JA, Mehta RL, Palevsky P. Acute renal failure—definition, outcome measures, animal models, fluid therapy and information technology needs: the Second International Consensus Conference of the Acute Dialysis Quality Initiative (ADQI) Group. Crit Care (London, England). 2004;8(4):R204–12.
Mehta RL, Kellum JA, Shah SV, Molitoris BA, Ronco C, Warnock DG, et al. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Crit Care (London, England). 2007;11(2):R31.
Kidney Disease: Improving Global Outcomes (KDIGO) Acute Kidney Injury Work Group. KDIGO Clinical Practice Guideline for Acute Kidney Injury. Kidney Int. 2012;Suppl(2):1–138.
Luther MK, Timbrook TT, Caffrey AR, Dosa D, Lodise TP, LaPlante KL. Vancomycin plus piperacillin-tazobactam and acute kidney injury in adults: a systematic review and meta-analysis. Crit Care Med. 2018;46(1):12–20.