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Intraoperative hyperglycemia in patients with an elevated preoperative C-reactive protein level may increase the risk of acute kidney injury after cardiac surgery

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A Letter to the Editor to this article was published on 09 April 2021

Abstract

Purpose

The effect of hyperglycemia on acute kidney injury (AKI) in patients undergoing cardiac surgery is unclear and may involve as yet unexplored factors. We hypothesized differential effects of intraoperative hyperglycemia on AKI after cardiac surgery depending on baseline inflammatory status, as reflected by the C-reactive protein (CRP) level.

Methods

This retrospective study included patients who underwent cardiac surgery seen at our hospital from 2008 to 2018. Patients were classified into four groups according to their preoperative CRP level (≥ 1 or < 1 mg/dl) and their intraoperative time-weighted average glucose concentration (> 140 or ≤ 140 mg/dl): low CRP and normoglycemia, low CRP and hyperglycemia, high CRP and normoglycemia, and high CRP and hyperglycemia. The data were analyzed by multivariable logistic regression analysis.

Results

The data of 3625 patients were analyzed. The logistic regression showed that patients in the high CRP and hyperglycemia group had a significantly higher risk of AKI than patients in the low CRP and normoglycemia group [odds ratio (OR), 1.58; 95% confidence interval (CI) 1.10–2.27], low CRP with hyperglycemia group (OR, 1.69; 95% CI 1.16–2.47) and high CRP with normoglycemia group (OR, 1.50; 95% CI 1.01–2.23).

Conclusions

Intraoperative hyperglycemia in patients with an elevated preoperative CRP level was significantly related to an increased risk of AKI after cardiac surgery. Individualized perioperative glycemic control may therefore be necessary in these patients.

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References

  1. Demirkilic U, Kuralay E, Yenicesu M, Caglar K, Oz BS, Cingoz F, Gunay C, Yildirim V, Ceylan S, Arslan M, Vural A, Tatar H. Timing of replacement therapy for acute renal failure after cardiac surgery. J Card Surg. 2004;19:17–20.

    Article  PubMed  Google Scholar 

  2. Provenchere S, Plantefeve G, Hufnagel G, Vicaut E, De Vaumas C, Lecharny JB, Depoix JP, Vrtovsnik F, Desmonts JM, Philip I. Renal dysfunction after cardiac surgery with normothermic cardiopulmonary bypass: incidence, risk factors, and effect on clinical outcome. Anesth Analg. 2003;96:1258–64.

    Article  PubMed  Google Scholar 

  3. Stallwood MI, Grayson AD, Mills K, Scawn ND. Acute renal failure in coronary artery bypass surgery: independent effect of cardiopulmonary bypass. Ann Thorac Surg. 2004;77:968–72.

    Article  PubMed  Google Scholar 

  4. Ostermann ME, Taube D, Morgan CJ, Evans TW. Acute renal failure following cardiopulmonary bypass: a changing picture. Intensive Care Med. 2000;26:565–71.

    Article  CAS  PubMed  Google Scholar 

  5. Ortega-Loubon C, Fernandez-Molina M, Carrascal-Hinojal Y, Fulquet-Carreras E. Cardiac surgery-associated acute kidney injury. Ann Card Anaesth. 2016;19:687–98.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Lagny MG, Jouret F, Koch JN, Blaffart F, Donneau AF, Albert A, Roediger L, Krzesinski JM, Defraigne JO. Incidence and outcomes of acute kidney injury after cardiac surgery using either criteria of the RIFLE classification. BMC Nephrol. 2015;16:76.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hobson C, Ozrazgat-Baslanti T, Kuxhausen A, Thottakkara P, Efron PA, Moore FA, Moldawer LL, Segal MS, Bihorac A. Cost and mortality associated with postoperative acute kidney injury. Ann Surg. 2015;261:1207–14.

    Article  PubMed  Google Scholar 

  8. Dasta JF, Kane-Gill SL, Durtschi AJ, Pathak DS, Kellum JA. Costs and outcomes of acute kidney injury (AKI) following cardiac surgery. Nephrol Dial Transplant. 2008;23:1970–4.

    Article  PubMed  Google Scholar 

  9. Billings FT 4th. Acute kidney injury following cardiac surgery: a clinical model. Nephron. 2019;143:202–6.

    Article  PubMed  Google Scholar 

  10. Billings FT 4th, Pretorius M, Schildcrout JS, Mercaldo ND, Byrne JG, Ikizler TA, Brown NJ. Obesity and oxidative stress predict AKI after cardiac surgery. J Am Soc Nephrol. 2012;23:1221–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Paller MS, Hoidal JR, Ferris TF. Oxygen free radicals in ischemic acute renal failure in the rat. J Clin Invest. 1984;74:1156–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Scrascia G, Guida P, Rotunno C, de Luca Tupputi Schinosa L, Paparella D. Anti-inflammatory strategies to reduce acute kidney injury in cardiac surgery patients: a meta-analysis of randomized controlled trials. Artif Organs. 2014;38:101–12.

    Article  CAS  PubMed  Google Scholar 

  13. Bonventre JV, Zuk A. Ischemic acute renal failure: an inflammatory disease? Kidney Int. 2004;66:480–5.

    Article  CAS  PubMed  Google Scholar 

  14. O'Neal JB, Shaw AD, Billings FT 4th. Acute kidney injury following cardiac surgery: current understanding and future directions. Crit Care. 2016;20:187.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Paparella D, Yau TM, Young E. Cardiopulmonary bypass induced inflammation: pathophysiology and treatment. An update Eur J Cardiothorac Surg. 2002;21:232–44.

    Article  CAS  PubMed  Google Scholar 

  16. Gordillo R, Ahluwalia T, Woroniecki R. Hyperglycemia and acute kidney injury in critically ill children. Int J Nephrol Renovasc Dis. 2016;9:201–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Song JW, Shim JK, Yoo KJ, Oh SY, Kwak YL. Impact of intraoperative hyperglycaemia on renal dysfunction after off-pump coronary artery bypass. Interact Cardiovasc Thorac Surg. 2013;17:473–8.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Ge QM, Dong Y, Zhang HM, Su Q. Effects of intermittent high glucose on oxidative stress in endothelial cells. Acta Diabetol. 2010;47(Suppl 1):97–103.

    Article  CAS  PubMed  Google Scholar 

  19. Maeda M, Hayashi T, Mizuno N, Hattori Y, Kuzuya M. Intermittent high glucose implements stress-induced senescence in human vascular endothelial cells: role of superoxide production by NADPH oxidase. PLoS ONE. 2015;10:e0123169.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Doenst T, Wijeysundera D, Karkouti K, Zechner C, Maganti M, Rao V, Borger MA. Hyperglycemia during cardiopulmonary bypass is an independent risk factor for mortality in patients undergoing cardiac surgery. J Thorac Cardiovasc Surg. 2005;130:1144.

    Article  PubMed  Google Scholar 

  21. Esposito K, Nappo F, Marfella R, Giugliano G, Giugliano F, Ciotola M, Quagliaro L, Ceriello A, Giugliano D. Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation. 2002;106:2067–72.

    Article  CAS  PubMed  Google Scholar 

  22. Lecomte P, Van Vlem B, Coddens J, Cammu G, Nollet G, Nobels F, Vanermen H, Foubert L. Tight perioperative glucose control is associated with a reduction in renal impairment and renal failure in non-diabetic cardiac surgical patients. Crit Care. 2008;12:R154.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Duncan AE, Abd-Elsayed A, Maheshwari A, Xu M, Soltesz E, Koch CG. Role of intraoperative and postoperative blood glucose concentrations in predicting outcomes after cardiac surgery. Anesthesiology. 2010;112:860–71.

    Article  PubMed  Google Scholar 

  24. Ouattara A, Lecomte P, Le Manach Y, Landi M, Jacqueminet S, Platonov I, Bonnet N, Riou B, Coriat P. Poor intraoperative blood glucose control is associated with a worsened hospital outcome after cardiac surgery in diabetic patients. Anesthesiology. 2005;103:687–94.

    Article  CAS  PubMed  Google Scholar 

  25. Furnary AP, Gao G, Grunkemeier GL, Wu Y, Zerr KJ, Bookin SO, Floten HS, Starr A. Continuous insulin infusion reduces mortality in patients with diabetes undergoing coronary artery bypass grafting. J Thorac Cardiovasc Surg. 2003;125:1007–211.

    Article  CAS  PubMed  Google Scholar 

  26. Kidney Disease: Improving Global Outcomes (KDIGO). Acute Kidney Injury Work Group. KDIGO clinical practice guideline for acute kidney injury. Kidney Int Suppl. 2012;2:1–138.

    Article  Google Scholar 

  27. Yoo S, Lee HJ, Lee H, Ryu HG. Association between perioperative hyperglycemia or glucose variability and postoperative acute kidney injury after liver transplantation: a retrospective observational study. Anesth Analg. 2017;124:35–41.

    Article  CAS  PubMed  Google Scholar 

  28. Kangasniemi OP, Biancari F, Luukkonen J, Vuorisalo S, Satta J, Pokela R, Juvonen T. Preoperative C-reactive protein is predictive of long-term outcome after coronary artery bypass surgery. Eur J Cardiothorac Surg. 2006;29:983–5.

    Article  PubMed  Google Scholar 

  29. Min JJ, Nam K, Kim TK, Kim HJ, Seo JH, Hwang HY, Kim KB, Murkin JM, Hong DM, Jeon Y. Relationship between early postoperative C-reactive protein elevation and long-term postoperative major adverse cardiovascular and cerebral events in patients undergoing off-pump coronary artery bypass graft surgery: a retrospective study. Br J Anaesth. 2014;113:391–401.

    Article  CAS  PubMed  Google Scholar 

  30. Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JGF, Coats AJS, Falk V, Gonzalez-Juanatey JR, Harjola VP, Jankowska EA, Jessup M, Linde C, Nihoyannopoulos P, Parissis JT, Pieske B, Riley JP, Rosano GMC, Ruilope LM, Ruschitzka F, Rutten FH, van der Meer P. 2016 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the task force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC) developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J. 2016;37:2129–200.

    Article  PubMed  Google Scholar 

  31. Curtis LH, Hammill BG, Eisenstein EL, Kramer JM, Anstrom KJ. Using inverse probability-weighted estimators in comparative effectiveness analyses with observational databases. Med Care. 2007;45:S103–S107107.

    Article  PubMed  Google Scholar 

  32. McCaffrey DF, Griffin BA, Almirall D, Slaughter ME, Ramchand R, Burgette LF. A tutorial on propensity score estimation for multiple treatments using generalized boosted models. Stat Med. 2013;32:3388–414.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Lazar HL, McDonnell M, Chipkin SR, Furnary AP, Engelman RM, Sadhu AR, Bridges CR, Haan CK, Svedjeholm R, Taegtmeyer H, Shemin RJ. Society of thoracic surgeons blood glucose guideline task force. The society of thoracic surgeons practice guideline series: blood glucose management during adult cardiac surgery. Ann Thorac Surg. 2009;87:663–9.

    Article  PubMed  Google Scholar 

  34. Gandhi GY, Nuttall GA, Abel MD, Mullany CJ, Schaff HV, O'Brien PC, Johnson MG, Williams AR, Cutshall SM, Mundy LM, Rizza RA, McMahon MM. Intensive intraoperative insulin therapy versus conventional glucose management during cardiac surgery: a randomized trial. Ann Intern Med. 2007;146:233–43.

    Article  PubMed  Google Scholar 

  35. NICE-SUGAR Study Investigators; Finfer S, Chittock DR, Su SY, Blair D, Foster D, Dhingra V, Bellomo R, Cook D, Dodek P, Henderson WR, Hebert PC, Heritier S, Heyland DK, McArthur C, McDonald E, Mitchell I, Myburgh JA, Norton R, Potter J, Robinson BG, Ronco JJ. Intensive versus conventional glucose control in critically ill patients. N Engl J Med. 2009;360:1283–97.

    Article  Google Scholar 

  36. Nyengaard JR, Ido Y, Kilo C, Williamson JR. Interactions between hyperglycemia and hypoxia: implications for diabetic retinopathy. Diabetes. 2004;53:2931–8.

    Article  CAS  PubMed  Google Scholar 

  37. Wang Z, do Carmo JM, Aberdein N, Zhou X, Williams JM, da Silva AA, Hall JE. Synergistic interaction of hypertension and diabetes in promoting kidney injury and the role of endoplasmic reticulum stress. Hypertension. 2017;69:879–91.

    Article  CAS  PubMed  Google Scholar 

  38. Yang X, Ko GT, So WY, Ma RC, Kong AP, Lam CW, Ho CS, Chow CC, Tong PC, Chan JC, Hong Kong Diabetes R. Additive interaction of hyperglycemia and albuminuria on risk of ischemic stroke in type 2 diabetes: Hong Kong Diabetes Registry. Diabetes Care. 2008;31:2294–300.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Krinsley JS, Preiser JC. Is it time to abandon glucose control in critically ill adult patients? Curr Opin Crit Care. 2019;25:299–306.

    Article  PubMed  Google Scholar 

  40. Ridker PM, Rifai N, Rose L, Buring JE, Cook NR. Comparison of C-reactive protein and low-density lipoprotein cholesterol levels in the prediction of first cardiovascular events. N Engl J Med. 2002;347:1557–655.

    Article  CAS  PubMed  Google Scholar 

  41. Ridker PM, Buring JE, Cook NR, Rifai N. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8 year follow-up of 14719 initially healthy American women. Circulation. 2003;107:391–7.

    Article  PubMed  Google Scholar 

  42. Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest. 2003;111:1805–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We specially thank Mr. Younghae Cho, B.S. (from the Department of Statistics, Sungkyunkwan University, Seoul, Korea) for his significant contribution to the statistical analyses of this work.

This study used clinical data retrieved from the Seoul National University Hospital Patients Research Environment (SUPREME) system.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: SL, YJ, and KN; Formal analysis and investigation: SL, SN, JB, YJC, and KN; Writing—original draft preparation: SL, SN, JB, YJC, and KN; Writing—review and editing: SN, JB, YJC, and KN; Supervision: YJ.

Corresponding author

Correspondence to Karam Nam.

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The authors have no conflicts of interest.

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Electronic supplementary material

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540_2020_2849_MOESM1_ESM.tif

Online Resource 1. Restricted cubic splines curve showing the log-odds for AKI following cardiac surgery according to preoperative CRP level. Three knots set at 10, 50, and 90 percentiles. AKI acute kidney injury, CRP C-reactive protein (TIF 443 kb)

540_2020_2849_MOESM2_ESM.tif

Online Resource 2. Restricted cubic splines curve showing the log-odds for AKI following cardiac surgery according to intraoperative TWAG. Three knots set at 10, 50, and 90 percentiles. AKI acute kidney injury, TWAG time-weighted average glucose concentration (TIF 480 kb)

Online Resource 3. Logistic regression analyses for acute kidney injury after cardiac surgery (DOCX 22 kb)

Online Resource 4. Multivariable logistic regression analyses stratified by preoperative Hemoglobin A1c (DOCX 15 kb)

Online Resource 5. Multivariable logistic regression performed using data of the last 5 years (DOCX 15 kb)

540_2020_2849_MOESM6_ESM.docx

Online Resource 6. Multivariable logistic regression performed in a subgroup where emergent surgeries were not included (DOCX 14 kb)

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Lee, S., Nam, S., Bae, J. et al. Intraoperative hyperglycemia in patients with an elevated preoperative C-reactive protein level may increase the risk of acute kidney injury after cardiac surgery. J Anesth 35, 10–19 (2021). https://doi.org/10.1007/s00540-020-02849-w

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  • DOI: https://doi.org/10.1007/s00540-020-02849-w

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