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Acute kidney injury in patients with cirrhosis: Acute Disease Quality Initiative (ADQI) and International Club of Ascites (ICA) joint multidisciplinary consensus meeting

Mitra K. Nadim, John A. Kellum, Lui Forni and 30 more

Journal of Hepatology · 2024 · Review · CC BY

doi:10.1016/j.jhep.2024.03.031

Abstract

Patients with cirrhosis are prone to developing acute kidney injury (AKI), a complication associated with a markedly increased in-hospital morbidity and mortality, along with a risk of progression to chronic kidney disease. Whereas patients with cirrhosis are at increased risk of developing any phenotype of AKI, hepatorenal syndrome (HRS), a specific form of AKI (HRS-AKI) in patients with advanced cirrhosis and ascites, carries an especially high mortality risk. Early recognition of HRS-AKI is crucial since administration of splanchnic vasoconstrictors may reverse the AKI and serve as a bridge to liver transplantation, the only curative option. In 2023, a joint meeting of the International Club of Ascites (ICA) and the Acute Disease Quality Initiative (ADQI) was convened to develop new diagnostic criteria for HRS-AKI, to provide graded recommendations for the work-up, management and post-discharge follow-up of patients with cirrhosis and AKI, and to highlight priorities for further research.

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    Palsson R, Colona MR, Hoenig MP, Assessment of interobserver reliability of nephrologist examination of urine sediment. JAMA Netw Open 2020;3(8):e2013959..

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    Jouet P, Meyrier A, Mal F, Transjugular renal biopsy in the treatment of patients with cirrhosis and renal abnormalities. Hepatology 1996;24(5):1143–1147..

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    Wadei HM, Heckman MG, Rawal B, Renal outcomes of liver transplant recipients who had pretransplant kidney biopsy. Transplantation 2014;98(12):1323–1330. (In eng).

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    Corapi KM, Chen JL, Balk EM, Gordon CE. Bleeding complications of native kidney biopsy: a systematic review and meta-analysis. Am J Kidney Dis 2012;60(1):62–73. (In eng).

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    Calmus Y, Conti F, Cluzel P, Prospective assessment of renal histopathological lesions in patients with end-stage liver disease: effects on long-term renal function after liver transplantation. J Hepatol 2012;57(3):572–576..

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  110. 110.

    Verna EC, Connelly C, Dove LM, Center-related bias in MELD scores within a liver transplant UNOS region: a call for standardization. Transplantation 2020;104(7):1396–1402..

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    Maiwall R, Kumar A, Bhardwaj A, Cystatin C predicts acute kidney injury and mortality in cirrhotics: a prospective cohort study. Liver Int 2018;38(4):654–664..

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    Markwardt D, Holdt L, Steib C, Plasma cystatin C is a predictor of renal dysfunction, acute-on-chronic liver failure, and mortality in patients with acutely decompensated liver cirrhosis. Hepatology 2017;66(4):1232–1241..

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    Slack AJ, McPhail MJ, Ostermann M, Predicting the development of acute kidney injury in liver cirrhosis–an analysis of glomerular filtration rate, proteinuria and kidney injury biomarkers. Aliment Pharmacol Ther 2013;37(10):989–997. (In eng).

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    Wan ZH, Wang JJ, You SL, Cystatin C is a biomarker for predicting acute kidney injury in patients with acute-on-chronic liver failure. World J Gastroenterol 2013;19(48):9432–9438. (In eng).

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    Jaques DA, Spahr L, Berra G, Biomarkers for acute kidney injury in decompensated cirrhosis: a prospective study. Nephrology (Carlton) 2019;24(2):170–180..

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    Barreto EF, Rule AD, Murad MH, Prediction of the renal elimination of drugs with cystatin C vs creatinine: a systematic review. Mayo Clin Proc 2019;94(3):500–514..

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    Singapura P, Ma TW, Sarmast N, Estimating glomerular filtration rate in cirrhosis using creatinine-based and cystatin C-based equations: systematic review and meta-analysis. Liver Transpl 2021;27(11):1538–1552..

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    Francoz C, Nadim MK, Baron A, Glomerular filtration rate equations for liver-kidney transplantation in patients with cirrhosis: validation of current recommendations. Hepatology 2014;59(4):1514–1521..

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    Delgado C, Baweja M, Crews DC, A unifying approach for GFR estimation: recommendations of the NKF-ASN task force on reassessing the inclusion of race in diagnosing kidney disease. J Am Soc Nephrol 2021;32(12):2994–3015..

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    Kalafateli M, Wickham F, Burniston M, Development and validation of a mathematical equation to estimate glomerular filtration rate in cirrhosis: the royal free hospital cirrhosis glomerular filtration rate. Hepatology 2017;65(2):582–591. (In eng).

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    Mindikoglu AL, Dowling TC, Magder LS, Estimation of glomerular filtration rate in patients with cirrhosis by using new and conventional filtration markers and dimethylarginines. Clin Gastroenterol Hepatol 2016;14(4):624–632.. (In eng).

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  122. 122.

    Asrani SK, Jennings LW, Trotter JF, A model for glomerular filtration rate assessment in liver disease (GRAIL) in the presence of renal dysfunction. Hepatology 2019;69(3):1219–1230..

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    Inker LA, Eneanya ND, Coresh J, New creatinine- and cystatin C-based equations to estimate GFR without race. N Engl J Med 2021;385(19):1737–1749. (In eng).

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    Panchal S, Serper M, Bittermann T, Impact of race-adjusted glomerular filtration rate estimation on eligibility for simultaneous liver-kidney transplantation. Liver Transpl 2022;28(6):959–968..

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    Proulx NL, Akbari A, Garg AX, Measured creatinine clearance from timed urine collections substantially overestimates glomerular filtration rate in patients with liver cirrhosis: a systematic review and individual patient meta-analysis. Nephrol Dial Transpl 2005;20(8):1617–1622..

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    Selistre L, de Souza V, Nicola C, Average creatinine-urea clearance: revival of an old analytical technique? Clin Kidney J 2023;16(8):1298–1306..

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    Murray PT, Mehta RL, Shaw A, Potential use of biomarkers in acute kidney injury: report and summary of recommendations from the 10th Acute Dialysis Quality Initiative consensus conference. Kidney Int 2014;85(3):513–521..

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    Treeprasertsuk S, Wongkarnjana A, Jaruvongvanich V, Urine neutrophil gelatinase-associated lipocalin: a diagnostic and prognostic marker for acute kidney injury (AKI) in hospitalized cirrhotic patients with AKI-prone conditions. BMC Gastroenterol 2015;15:140..

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    Lima C, Gorab DL, Fernandes CR, Role of proenkephalin in the diagnosis of severe and subclinical acute kidney injury during the perioperative period of liver transplantation. Pract Lab Med 2022;31:e00278..

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    Jo SK, Yang J, Hwang SM, Role of biomarkers as predictors of acute kidney injury and mortality in decompensated cirrhosis. Sci Rep 2019;9(1): 14508..

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    McCullough PA, Shaw AD, Haase M, Diagnosis of acute kidney injury using functional and injury biomarkers: workgroup statements from the tenth Acute Dialysis Quality Initiative Consensus Conference. Contrib Nephrol 2013;182:13–29..

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    Asrani SK, Shankar N, da Graca B, Role of novel kidney biomarkers in patients with cirrhosis and after liver transplantation. Liver Transpl 2022;28(3):466–482..

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    Juanola A, Ma AT, Pose E, Gines P. Novel biomarkers of AKI in cirrhosis. Semin Liver Dis 2022;42(4):489–500..

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    Fagundes C, Pepin MN, Guevara M, Urinary neutrophil gelatinase-associated lipocalin as biomarker in the differential diagnosis of impairment of kidney function in cirrhosis. J Hepatol 2012;57(2):267–273..

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    Lei L, Li LP, Zeng Z, Value of urinary KIM-1 and NGAL combined with serum Cys C for predicting acute kidney injury secondary to decompensated cirrhosis. Sci Rep 2018;8(1):7962..

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    Finfer S, Bellomo R, Boyce N, A comparison of albumin and saline for fluid resuscitation in the intensive care unit. N Engl J Med 2004;350(22):2247–2256..

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    Caironi P, Tognoni G, Masson S, Albumin replacement in patients with severe sepsis or septic shock. N Engl J Med 2014;370(15):1412–1421..

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    Alcaraz-Quiles J, Casulleras M, Oettl K, Oxidized albumin triggers a cytokine storm in leukocytes through P38 mitogen-activated Protein kinase: role in systemic inflammation in decompensated cirrhosis. Hepatology 2018;68(5):1937–1952..

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    Arroyo V, Garcia-Martinez R, Salvatella X. Human serum albumin, systemic inflammation, and cirrhosis. J Hepatol 2014;61(2):396–407..

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    Maiwall R, Kumar A, Pasupuleti SSR, A randomized-controlled trial comparing 20% albumin to plasmalyte in patients with cirrhosis and sepsis-induced hypotension [ALPS trial]. J Hepatol 2022;77(3):670–682. (In eng).

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    Philips CA, Maiwall R, Sharma MK, Comparison of 5% human albumin and normal saline for fluid resuscitation in sepsis induced hypotension among patients with cirrhosis (FRISC study): a randomized controlled trial. Hepatol Int 2021;15(4):983–994. (In eng).

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    Umgelter A, Reindl W, Wagner KS, Effects of plasma expansion with albumin and paracentesis on haemodynamics and kidney function in critically ill cirrhotic patients with tense ascites and hepatorenal syndrome: a prospective uncontrolled trial. Crit Care 2008;12(1):R4. (In eng).

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    Umgelter A, Reindl W, Franzen M, Renal resistive index and renal function before and after paracentesis in patients with hepatorenal syndrome and tense ascites. Intensive Care Med 2009;35(1):152–156..

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    Pozzi M, Osculati G, Boari G, Time course of circulatory and humoral effects of rapid total paracentesis in cirrhotic patients with tense, refractory ascites. Gastroenterology 1994;106(3):709–719..

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    Seethapathy H, Sharma S, Zhao S, Acute kidney injury following paracentesis among inpatients with cirrhosis. Kidney Int Rep 2020;5(8):1305–1308. (In eng).

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    Ginés P, Arroyo V, Quintero E, Comparison of paracentesis and diuretics in the treatment of cirrhotics with tense ascites. Results of a randomized study. Gastroenterology 1987;93(2):234–241. (In eng).

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    Gaudry S, Hajage D, Schortgen F, Initiation strategies for renal-replacement therapy in the intensive care unit. N Engl J Med 2016;375(2):122–133. (In eng).

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    Barbar SD, Clere-Jehl R, Bourredjem A, Timing of renal-replacement therapy in patients with acute kidney injury and sepsis. N Engl J Med 2018;379(15):1431–1442. (In eng).

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    Wald R, Bagshaw SM. Timing of initiation of renal-replacement therapy in acute kidney injury. Reply N Engl J Med 2020;383(18):1797–1798. (In eng).

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    Bouchard J, Mehta RL. Timing of kidney support therapy in acute kidney injury: what are we waiting for? Am J Kidney Dis 2022;79(3):417–426..

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    Ostermann M, Joannidis M, Pani A, Patient selection and timing of continuous renal replacement therapy. Blood Purif 2016;42(3):224–237..

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    Rosner MH, Ostermann M, Murugan R, Indications and management of mechanical fluid removal in critical illness. Br J Anaesth 2014;113(5):764–771..

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    Nadim MK, DiNorcia J, Ji L, Inequity in organ allocation for patients awaiting liver transplantation: rationale for uncapping the model for end-stage liver disease. J Hepatol 2017;67(3):517–525..

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    Scherer JS, Holley JL. The role of time-limited trials in dialysis decision making in critically ill patients. Clin J Am Soc Nephrol 2016;11(2):344–353. (In eng).

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    Braun HJ, Mello A, Kothari R, Expedited evaluation for liver transplantation: a critical look at processes and outcomes. Clin Transpl 2022;36(3):e14539..

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    Dong V, Nadim MK, Karvellas CJ. Post-liver transplant acute kidney injury. Liver Transpl 2021;27(11):1653–1664..

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    Nadim MK, Sung RS, Davis CL, Simultaneous liver-kidney transplantation summit: current state and future directions. Am J Transpl 2012;12(11):2901–2908..

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    Levitsky J, Baker T, Ahya SN, Outcomes and native renal recovery following simultaneous liver-kidney transplantation. Am J Transpl 2012;12(11):2949–2957..

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    U.S. Department of Health & Human Services: organ procurement and transplantation network data. Available at: https://optn.transplant.hrsa.gov/data.

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    Nadim MK, Genyk YS, Tokin C, Impact of the etiology of acute kidney injury on outcomes following liver transplantation: acute tubular necrosis versus hepatorenal syndrome. Liver Transpl 2012;18(5):539–548..

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    Levitsky J, Asrani SK, Klintmalm G, Discovery and validation of a biomarker model (PRESERVE) predictive of renal outcomes after liver transplantation. Hepatology 2020;71(5):1775–1786..

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    Levitsky J, Asrani SK, Abecassis M, External validation of a pretransplant biomarker model (REVERSE) predictive of renal recovery after liver transplantation. Hepatology 2019;70(4):1349–1359..

    Not in our library10.1002/hep.30667

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    Dodge JL, Lee BT, Kassem ACZ, The conundrum of patients with compensated cirrhosis requiring kidney transplantation; kidney alone or simultaneous liver kidney transplantation. Transplantation 2023;107(2):429–437..

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    Allegretti AS, Ortiz G, Cui J, Changes in kidney function after transjugular intrahepatic portosystemic shunts versus large-volume paracentesis in cirrhosis: a matched cohort analysis.. The Official Journal of the National Kidney Foundation Am J Kidney Dis 2016. S0272-S6386(16)00211–0 [pii].

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    Charilaou P, Devani K, Petrosyan R, Inpatient mortality benefit with transjugular intrahepatic portosystemic shunt for hospitalized hepatorenal syndrome patients. Dig Dis Sci 2020;65(11):3378–3388..

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    Ponzo P, Campion D, Rizzo M, Transjugular intrahepatic portosystemic shunt in cirrhotic patients with hepatorenal syndrome - chronic kidney disease: impact on renal function. Dig Liver Dis 2022;54(8):1101–1108..

    Not in our library10.1016/j.dld.2021.09.008

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    Song T, Rossle M, He F, Transjugular intrahepatic portosystemic shunt for hepatorenal syndrome: a systematic review and meta-analysis. Dig Liver Dis 2018;50(4):323–330..

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    Guevara M, Gines P, Bandi JC, Transjugular intrahepatic portosystemic shunt in hepatorenal syndrome: effects on renal function and vasoactive systems. Hepatology 1998;28(2):416–422..

    Not in our library10.1002/hep.510280219

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    Ripoll C, Platzer S, Franken P, Liver-HERO: hepatorenal syndrome-acute kidney injury (HRS-AKI) treatment with transjugular intrahepatic portosystemic shunt in patients with cirrhosis-a randomized controlled trial. Trials 2023;24(1):258..

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    Kribben A, Gerken G, Haag S, Effects of fractionated plasma separation and adsorption on survival in patients with acute-on-chronic liver failure. Gastroenterology 2012;142(4):782–789 e3..

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    Niewinski G, Raszeja-Wyszomirska J, Hrenczuk M, Intermittent high-flux albumin dialysis with continuous venovenous hemodialysis for acute-on-chronic liver failure and acute kidney injury. Artif Organs 2020;44(1):91–99..

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    Agarwal B, Canizares RB, Saliba F, Randomized, controlled clinical trial of the DIALIVE liver dialysis device versus standard of care in patients with acute-on-chronic liver failure. J Hepatol 2023;79(1):79–92..

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    Popescu M, David C, Marcu A, Artificial liver support with CytoSorb and MARS in liver failure: a retrospective propensity matched analysis. J Clin Med 2023;12(6)..

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    Cavallin M, Piano S, Romano A, Terlipressin given by continuous intravenous infusion versus intravenous boluses in the treatment of hepatorenal syndrome: a randomized controlled study. Hepatology 2016;63(3):983–992. (In eng).

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    Facciorusso A, Chandar AK, Murad MH, Comparative efficacy of pharmacological strategies for management of type 1 hepatorenal syndrome: a systematic review and network meta-analysis. Lancet Gastroenterol Hepatol 2017;2(2):94–102..

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    Pitre T, Kiflen M, Helmeczi W, The comparative effectiveness of vasoactive treatments for hepatorenal syndrome: a systematic review and network meta-analysis. Crit Care Med 2022;50(10):1419–1429..

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    Best LM, Freeman SC, Sutton AJ, Treatment for hepatorenal syndrome in people with decompensated liver cirrhosis: a network meta-analysis. Cochrane Database Syst Rev 2019;9(9):CD013103..

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    Arora V, Maiwall R, Rajan V, Terlipressin is superior to noradrenaline in the management of acute kidney injury in acute on chronic liver failure. Hepatology 2020;71(2):600–610..

    Not in our library10.1002/hep.30208

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    Cavallin M, Kamath PS, Merli M, Terlipressin plus albumin versus midodrine and octreotide plus albumin in the treatment of hepatorenal syndrome: a randomized trial. Hepatology (Baltimore, Md) 2015;62(2):567–574..

    Not in our library10.1002/hep.27709

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    El-Desoki Mahmoud EI, Abdelaziz DH, Abd-Elsalam S, Norepinephrine is more effective than midodrine/octreotide in patients with hepatorenal syndrome-acute kidney injury: a randomized controlled trial. Front Pharmacol 2021;12:675948..

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    Velez JCQ, Karakala N, Tayebi K, Responsiveness to vasoconstrictor therapy in hepatorenal syndrome type 1. Kidney360 2023;4(4):e448–e456..

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    Velez JC, Kadian M, Taburyanskaya M, Hepatorenal acute kidney injury and the importance of raising mean arterial pressure. Nephron 2015;131(3):191–201. (In eng).

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    Moore K, Jamil K, Verleger K, Real-world treatment patterns and outcomes using terlipressin in 203 patients with the hepatorenal syndrome. Aliment Pharmacol Ther 2020..

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    Maddukuri G, Cai CX, Munigala S, Targeting an early and substantial increase in mean arterial pressure is critical in the management of type 1 hepatorenal syndrome: a combined retrospective and pilot study. Dig Dis Sci 2014;59(2):471–481..

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    Sanyal AJ, Boyer T, Garcia-Tsao G, A randomized, prospective, double-blind, placebo-controlled trial of terlipressin for type 1 hepatorenal syndrome. Gastroenterology 2008;134(5):1360–1368..

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    Martín-Llahí M, Pépin MN, Guevara M, Terlipressin and albumin vs albumin in patients with cirrhosis and hepatorenal syndrome: a randomized study. Gastroenterology 2008;134(5):1352–1359. (In eng).

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    Boyer TD, Sanyal AJ, Wong F, Terlipressin plus albumin is more effective than albumin alone in improving renal function in patients with cirrhosis and hepatorenal syndrome type 1. Gastroenterology 2016;150(7):1579–1589 e2..

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    Wong F, Pappas SC, Curry MP, Terlipressin plus albumin for the treatment of type 1 hepatorenal syndrome. N Engl J Med 2021;384(9):818–828. (In eng).

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    Pichler RH, Swenson ER, Leary PJ, Terlipressin: hopes fulfilled or dashed? Clin J Am Soc Nephrol 2022;17(1):140–142..

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    Allegretti AS, Subramanian RM, Francoz C, Respiratory events with terlipressin and albumin in hepatorenal syndrome: a review and clinical guidance. Liver Int 2022;42(10):2124–2130. (In eng).

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    Piano S, Gambino C, Vettore E, Response to terlipressin and albumin is associated with improved liver transplant outcomes in patients with hepatorenal syndrome. Hepatology 2021;73(5):1909–1919. (In eng).

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    Angeli P, Gines P. Hepatorenal syndrome, MELD score and liver transplantation: an evolving issue with relevant implications for clinical practice. J Hepatol 2012;57(5):1135–1140. (In eng).

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    Kellum JA, Sileanu FE, Bihorac A, Recovery after acute kidney injury. Am J Respir Crit Care Med 2017;195(6):784–791. (In eng).

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    Harel Z, Wald R, Bargman JM, Nephrologist follow-up improves all-cause mortality of severe acute kidney injury survivors. Kidney Int 2013;83(5):901–908. (In eng).

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    Ly H, Ortiz-Soriano V, Liu LJ, Characteristics and outcomes of survivors of critical illness and acute kidney injury followed in a pilot acute kidney injury clinic. Kidney Int Rep 2021;6(12):3070–3073..

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    Singh G, Hu Y, Jacobs S, Post-discharge mortality and rehospitalization among participants in a comprehensive acute kidney injury rehabilitation program. Kidney360 2021;2(9):1424–1433..

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    See EJ, Jayasinghe K, Glassford N, Long-term risk of adverse outcomes after acute kidney injury: a systematic review and meta-analysis of cohort studies using consensus definitions of exposure. Kidney Int 2019;95(1):160–172..

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    Mindikoglu AL, Hernaez R, Liu Y, Renal trajectory patterns are associated with postdischarge mortality in patients with cirrhosis and acute kidney injury. Clin Gastroenterol Hepatol 2020;18(8):1858–1866 e6..

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    Bajaj JS, Reddy KR, Tandon P, The 3-month readmission rate remains unacceptably high in a large North American cohort of patients with cirrhosis. Hepatology 2016;64(1):200–208..

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    de Franchis R, Bosch J, Garcia-Tsao G, Baveno VII - renewing consensus in portal hypertension. J Hepatol 2022;76(4):959–974. (In eng).

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    Gharaibeh KA, Hamadah AM, El-Zoghby ZM, Cystatin C predicts renal recovery earlier than creatinine among patients with acute kidney injury. Kidney Int Rep 2018;3(2):337–342..

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