Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T02:19:21.773Z Has data issue: false hasContentIssue false
  • English
  • Français

Post-operative acute kidney injury is associated with a biomarker of acute brain injury after paediatric cardiac surgery

Published online by Cambridge University Press:  30 March 2020

Michael Parsons Open the ORCID record for Michael Parsons [Opens in a new window] ,
Jason Greenberg ,
Chirag Parikh ,
Jeremiah Brown ,
Devin Parker ,
Jie Zhu ,
Luca Vricella  and
Allen D. Everett
Michael Parsons*
Affiliation:
Department of Pediatrics, The Helen B. Taussig Congenital Heart Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA
Jason Greenberg
Affiliation:
Department of Pediatrics, Yale School of Medicine, New Haven, CT, USA
Chirag Parikh
Affiliation:
Department of Pediatrics, The Helen B. Taussig Congenital Heart Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA
Jeremiah Brown
Affiliation:
Department of Epidemiology, Dartmouth Geisel School of Medicine, Hanover, NH, USA
Devin Parker
Affiliation:
Department of Epidemiology, Dartmouth Geisel School of Medicine, Hanover, NH, USA
Jie Zhu
Affiliation:
Department of Pediatrics, The Helen B. Taussig Congenital Heart Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA
Luca Vricella
Affiliation:
Department of Pediatric Cardiac Surgery, University of Chicago School of Medicine, Chicago, IL, USA
Allen D. Everett
Affiliation:
Department of Pediatrics, The Helen B. Taussig Congenital Heart Center, Johns Hopkins University School of Medicine, Baltimore, MD, USA
*
Author for correspondence: M. Parsons, Johns Hopkins Pediatric Cardiology, Johns Hopkins University, 1800 Orleans St., Room 2201, Baltimore, MD21287, USA. Tel: (240) 603 9918; Fax: (410) 955 0897; E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Introduction:

Children with CHD who undergo cardiopulmonary bypass are at an increased risk of acute kidney injury. This study evaluated the association of end-organ specific injury plasma biomarkers for brain: glial fibrillary acidic protein and heart: Galectin 3, soluble suppression of tumorgenicity 2, and N-terminal pro b-type natriuretic peptide with acute kidney injury in children undergoing cardiopulmonary bypass.

Materials and Methods:

We enrolled consecutive children undergoing cardiac surgery with cardiopulmonary bypass. Blood samples were collected pre-bypass in the operating room and in the immediate post-operative period. Acute kidney injury was defined as a rise of serum creatinine ≥50% from pre-operative baseline within 7 days after surgery.

Results:

Overall, 162 children (mean age 4.05 years, sd 5.28 years) were enrolled. Post-operative acute kidney injury developed in 55 (34%) children. Post-operative plasma glial fibrillary acidic protein levels were significantly higher in patients with acute kidney injury (median 0.154 (inter-quartile range 0.059–0.31) ng/ml) compared to those without acute kidney injury (median 0.056 (inter-quartile range 0.001–0.125) ng/ml) (p = 0.043). After adjustment for age, weight, and The Society of Thoracic Surgeons-European Association for Cardio-Thoracic Surgery category, each natural log increase in post-operative glial fibrillary acidic protein was significantly associated with a higher risk for subsequent acute kidney injury (adjusted odds ratio glial fibrillary acidic protein 1.25; 95% confidence interval 1.01–1.59). Pre/post-operative levels of galectin 3, soluble suppression of tumorgenicity 2, and N-terminal pro b-type natriuretic peptide did not significantly differ between patients with and without acute kidney injury.

Conclusions:

Higher plasma glial fibrillary acidic protein levels measured in the immediate post-operative period were independently associated with subsequent acute kidney injury in children after cardiopulmonary bypass. Elevated glial fibrillary acidic protein likely reflects intraoperative brain injury which may occur in the context of acute kidney injury-associated end-organ dysfunction.

Keywords

Cardiologybypasskidneybiomarker
Type
Original Article
Information
Cardiology in the Young , Volume 30 , Issue 4 , April 2020 , pp. 505 - 510
Copyright
© The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Van Der Linde, D, Konings, EEM, Slager, MA, et al.Birth prevalence of congenital heart disease worldwide: a systematic review and meta-analysis. J Am Coll Cardiol 2011; 58: 2241–2247.10.1016/j.jacc.2011.08.025CrossRefGoogle ScholarPubMed
Yang, Q, Chen, H, Correa, A, et al.Racial differences in infant mortality attributable to birth defects in the United States, 1989-2002. Birth Defects Res Part A - Clin Mol Teratol 2006; 76: 706–713.10.1002/bdra.20308CrossRefGoogle ScholarPubMed
Moller, JH, Taubert, KA, Allen, HD, et al.AHA medical/scientific statement special report cardiovascular health and disease in children : current status. Circulation 1994; 89: 8–10.Google Scholar
Li, S, Krawczeski, C, Zappitelli, M, et al.Incidence, risk factors, and outcomes of acute kidney injury after pediatric cardiac surgery – a prospective multicenter study. Crit Care Med 2012; 39: 1493–1499.10.1097/CCM.0b013e31821201d3CrossRefGoogle Scholar
Shaw, NJ, Brocklebank, JT, Dickinson, DF, et al.Long-term outcome for children with acute renal failure following cardiac surgery. Int J Cardiol 1991; 31: 161–165.CrossRefGoogle ScholarPubMed
Greenberg, JH, Coca, S, Parikh, CR. Long-term risk of chronic kidney disease and mortality in children after acute kidney injury : a systematic review. BMC Nephrol 2014; 15: 184.CrossRefGoogle ScholarPubMed
Panickar, KS, Noremberg, MD. Astrocytes in cerebral ischemic injury: morphological and general considerations. Glia 2005; 50: 287–298.10.1002/glia.20181CrossRefGoogle ScholarPubMed
Herrmann, M, Vos, P, Wunderlich, MT, et al.Release of glial tissue – specific proteins after acute stroke. Stroke 2000; 31: 2670–2677.10.1161/01.STR.31.11.2670CrossRefGoogle ScholarPubMed
Kaneko, T, Kasaoka, S, Miyauchi, T, et al.Serum glial fibrillary acidic protein as a predictive biomarker of neurological outcome after cardiac arrest. Resuscitation 2009; 80: 790–794.10.1016/j.resuscitation.2009.04.003CrossRefGoogle ScholarPubMed
Vedovelli, L, Padalino, M, Suppiej, A, et al.Cardiopulmonary-bypass glial fibrillary neurocognitive skills. Ann Thorac Surg 2018; 106: 792–798.10.1016/j.athoracsur.2018.03.083CrossRefGoogle ScholarPubMed
Graham, E, Martin, R, Atz, A, et al.Association of intraoperative circulating-brain injury biomarker and neurodevelopmental outcomes at 1 year among neonates undergoing cardiac surgery. J Thorac Cardiovasc Surg 2019; 157: 1996–2002.10.1016/j.jtcvs.2019.01.040CrossRefGoogle Scholar
Bembea, MM, Savage, W, Strouse, JJ, et al.Glial febrillary acidic protein as a brain injury biomarker in children undergoing extracorporeal membrane oxygenation. Pedaitr Crit Care Med 2013; 12: 572–579.10.1097/PCC.0b013e3181fe3ec7CrossRefGoogle Scholar
Frunza, O, Russo, I, Saxena, A, et al.Myocardial galectin-3 expression is associated with remodeling of the pressure-overloaded heart and may delay the hypertrophic response without affecting survival, dysfunction, and cardiac fibrosis. Am J Pathol 2016; 186: 1114–1127.10.1016/j.ajpath.2015.12.017CrossRefGoogle ScholarPubMed
van Kimmenade, RR, Januzzi, JL, Ellinor, PT, et al.Utility of amino-terminal pro-brain natriuretic peptide, galectin-3, and apelin for the evaluation of patients with acute heart failure. J Am Coll Cardiol 2006; 48: 1217–1224.10.1016/j.jacc.2006.03.061CrossRefGoogle ScholarPubMed
Lok, DJ, Lok, SI, De La Porte, PW Bruggink-André, et al.Galectin-3 is an independent marker for ventricular remodeling and mortality in patients with chronic heart failure. Clin Res Cardiol 2013; 102: 103–110.CrossRefGoogle ScholarPubMed
Ballmoos, MW Von, Likosky, DS, Rezaee, M, et al.Elevated preoperative Galectin-3 is associated with acute kidney injury after cardiac surgery. BMC Nephrol 2018; 19: 280.10.1186/s12882-018-1093-0CrossRefGoogle Scholar
Ciccone, MM, Cortese, F, Gesualdo, M, et al.A novel cardiac bio-marker: ST2: a review. Molecules 2013; 18: 15314–15328.10.3390/molecules181215314CrossRefGoogle ScholarPubMed
Sanada, S, Hakuno, D, Higgins, LJ, et al.IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system. J Clin Invest 2007; 117: 1538–1549.10.1172/JCI30634CrossRefGoogle ScholarPubMed
Januzzi, JL. ST2 as a cardiovascular risk biomarker: from the bench to the bedside. J Cardiovasc Transl Res 2013; 6: 493–500.10.1007/s12265-013-9459-yCrossRefGoogle Scholar
Lobdell, KW, Parker, DM, Likosky, DS, et al.Preoperative serum ST2 level predicts acute kidney injury after adult cardiac surgery. J Thorac Cardiovasc Surg 2018; 156: 1114–1123.e2.10.1016/j.jtcvs.2018.03.149CrossRefGoogle ScholarPubMed
Januzzi, JL, Van Kimmenade, R, Lainchbury, J, et al.NT-proBNP testing for diagnosis and short-term prognosis in acute destabilized heart failure: an international pooled analysis of 1256 patients: the international collaborative of NT-proBNP study. Eur Heart J 2006; 27: 330–337.10.1093/eurheartj/ehi631CrossRefGoogle ScholarPubMed
Patel, UD, Garg, AX, Krumholz, HM, et al.Preoperative serum brain natriuretic peptide and risk of acute kidney injury after cardiac surgery. Circulation 2012; 125: 1347–1355.10.1161/CIRCULATIONAHA.111.029686CrossRefGoogle ScholarPubMed
Bucholz, EM, Whitlock, RP, Zappitelli, M, et al.Cardiac biomarkers and acute kidney injury after cardiac surgery. Pediatrics 2015; 135: e945–e956.CrossRefGoogle ScholarPubMed
Petzold, A, Keir, G, Green, AJE, et al.An ELISA for glial fibrillary acidic protein. J Immunol Methods 2004; 287: 169–177.10.1016/j.jim.2004.01.015CrossRefGoogle ScholarPubMed
Savage, WJ, Barron-Casella, E, Fu, Z, et al.Plasma glial fibrillary acidic protein levels in children with sickle cell disease. Am J Hematol 2011; 86: 427–429.10.1002/ajh.21995CrossRefGoogle ScholarPubMed
Rosengren, L, Ahlsen, G, Belfrage, M, et al.A sensitive ELISA for glial fibrillary acidic protein: application in CSF in children. J Neurosci Methods 1992; 44: 113–119.10.1016/0165-0270(92)90004-WCrossRefGoogle Scholar
Ennen, CS, Huisman, TAGM, Savage, WJ, et al.Glial fibrillary acidic protein as a biomarker for neonatal hypoxic-ischemic encephalopathy treated with whole-body cooling. Am J Obstet Gynecol 2011; 205: 251.e1-7.10.1016/j.ajog.2011.06.025CrossRefGoogle ScholarPubMed
Brunetti, MA, Jennings, JM, Easley, RB, et al.Glial fibrillary acidic protein in children with congenital heart disease undergoing cardiopulmonary bypass. Cardiol Young 2014; 24: 623–631.10.1017/S1047951113000851CrossRefGoogle ScholarPubMed
Hori, D, Everett, AD, Lee, JK, et al.Rewarming rate during cardiopulmonary bypass is associated with release of glial fibrillary acidic protein. Ann Thorac Surg 2015; 100: 1353–1358.10.1016/j.athoracsur.2015.04.006CrossRefGoogle ScholarPubMed
Molitoris, BA, Levin, A, Warnock, DG, et al.Improving outcomes of acute kidney injury: report of an initiative. Nat Clin Pract Nephrol 2007; 3: 439–442.10.1038/ncpneph0551CrossRefGoogle ScholarPubMed
Jacobs, JP, Mayer, JE, Mavroudis, C, et al.The society of thoracic surgeons congenital heart surgery database: 2016 update on outcomes and quality. Ann Thorac Surg 2016; 101: 850–862.10.1016/j.athoracsur.2016.01.057CrossRefGoogle Scholar
Limperopoulos, C, Majnemer, A, Shevell, MI, et al.Neurodevelopmental status of newborns and infants with congenital heart defects before and after open heart surgery. J Pediatr 2000; 137: 638–645.CrossRefGoogle ScholarPubMed
Gaynor, JW, Stopp, C, Wypij, D, et al.Neurodevelopmental outcomes after cardiac surgery in infancy. Pediatrics 2015; 135: 816–825.10.1542/peds.2014-3825CrossRefGoogle ScholarPubMed
O’Neal, JB, Shaw, AD, Billings, FT. Acute kidney injury following cardiac surgery: current understanding and future directions. Crit Care 2016; 20: 1–9.10.1186/s13054-016-1352-zCrossRefGoogle ScholarPubMed
Ricksten, SE, Bragadottir, G, Redfors, B. Renal oxygenation in clinical acute kidney injury. Crit Care 2013; 17: 221.10.1186/cc12530CrossRefGoogle ScholarPubMed
Billings, FT, Yu, C, Byrne, JG, et al.Heme oxygenase-1 and acute kidney injury following cardiac surgery. Cardiorenal Med 2014; 4: 12–21.10.1159/000357871CrossRefGoogle ScholarPubMed
Zhang, WR, Garg, AX, Coca, SG, et al.Plasma IL-6 and IL-10 concentrations predict AKI and long-term mortality in adults after cardiac surgery. J Am Soc Nephrol 2015; 26: 3123–3132.10.1681/ASN.2014080764CrossRefGoogle ScholarPubMed
Ruf, B, Bonelli, V, Balling, G, et al.Intraoperative renal near-infrared spectroscopy indicates developing acute kidney injury in infants undergoing cardiac surgery with cardiopulmonary bypass : a case – control study. Crit Care 2015; 19: 1–11.10.1186/s13054-015-0760-9CrossRefGoogle ScholarPubMed
Ky, B, French, B, Mccloskey, K, et al.High-sensitivity ST2 for prediction of adverse outcomes in chronic heart failure. Circ Heart Fail 2011; 4: 180–187.10.1161/CIRCHEARTFAILURE.110.958223CrossRefGoogle ScholarPubMed
Bayes-genis, A, Pascual-figal, D, Januzzi, JL, et al.Soluble ST2 monitoring provides additional risk stratification for outpatients with decompensated heart failure. Rev Esp Cardiol 2010; 63: 1171–1178.10.1016/S0300-8932(10)70249-9CrossRefGoogle ScholarPubMed
Schachner, T, Wiedemann, ID, Fetz, IIH, et al.Influence of preoperative serum N-terminal pro-brain type natriuretic peptide on the postoperative outcome and survival rates of coronary artery bypass patients. Clinics (Sao Paulo) 2010; 65: 1239–1245.10.1590/S1807-59322010001200004CrossRefGoogle ScholarPubMed
Cohn, JN, Ferrari, R, Sharpe, N, et al.Cardiac remodeling — concepts and clinical implications : a consensus paper from an international forum on cardiac remodeling. J Am Coll Cardiol 2000; 35: 569–582.10.1016/S0735-1097(99)00630-0CrossRefGoogle ScholarPubMed