Anaerobic Lactate Production Is Associated With Decreased Microcirculatory Blood Flow and Decreased Mitochondrial Respiration Following Cardiovascular Surgery With Cardiopulmonary Bypass.


Journal

Critical care medicine
ISSN: 1530-0293
Titre abrégé: Crit Care Med
Pays: United States
ID NLM: 0355501

Informations de publication

Date de publication:
05 Apr 2024
Historique:
medline: 5 4 2024
pubmed: 5 4 2024
entrez: 5 4 2024
Statut: aheadofprint

Résumé

Quantify the relationship between perioperative anaerobic lactate production, microcirculatory blood flow, and mitochondrial respiration in patients after cardiovascular surgery with cardiopulmonary bypass. Serial measurements of lactate-pyruvate ratio (LPR), microcirculatory blood flow, plasma tricarboxylic acid cycle cycle intermediates, and mitochondrial respiration were compared between patients with a normal peak lactate (≤ 2 mmol/L) and a high peak lactate (≥ 4 mmol/L) in the first 6 hours after surgery. Regression analysis was performed to quantify the relationship between clinically relevant hemodynamic variables, lactate, LPR, and microcirculatory blood flow. This was a single-center, prospective observational study conducted in an academic cardiovascular ICU. One hundred thirty-two patients undergoing elective cardiovascular surgery with cardiopulmonary bypass. None. Patients with a high postoperative lactate were found to have a higher LPR compared with patients with a normal postoperative lactate (14.4 ± 2.5 vs. 11.7 ± 3.4; p = 0.005). Linear regression analysis found a significant, negative relationship between LPR and microcirculatory flow index (r = -0.225; β = -0.037; p = 0.001 and proportion of perfused vessels: r = -0.17; β = -0.468; p = 0.009). There was not a significant relationship between absolute plasma lactate and microcirculation variables. Last, mitochondrial complex I and complex II oxidative phosphorylation were reduced in patients with high postoperative lactate levels compared with patients with normal lactate (22.6 ± 6.2 vs. 14.5 ± 7.4 pmol O2/s/106 cells; p = 0.002). Increased anaerobic lactate production, estimated by LPR, has a negative relationship with microcirculatory blood flow after cardiovascular surgery. This relationship does not persist when measuring lactate alone. In addition, decreased mitochondrial respiration is associated with increased lactate after cardiovascular surgery. These findings suggest that high lactate levels after cardiovascular surgery, even in the setting of normal hemodynamics, are not simply a type B phenomenon as previously suggested.

Identifiants

pubmed: 38578158
doi: 10.1097/CCM.0000000000006289
pii: 00003246-990000000-00322
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 by the Society of Critical Care Medicine and Wolters Kluwer Health, Inc. All Rights Reserved.

Déclaration de conflit d'intérêts

Drs. Greenwood, Jang, and Brenner received support for article research from the National Institutes of Health. Dr. Greenwood is supported by the National Center for Advancing Translational Sciences (award number KL2TR001879). Dr. Jang is supported by the National Heart, Lung, and Blood Institute (NHLBI; award number R01HL166592). Dr. Acker received funding from FineHeart. Dr. Kilbaugh is supported by the National Institutes of Congenital Heart Disease (award number R01HL141386). Dr. Brenner is supported by the NHLBI (award number R01HL153510). Dr. Brenner’s institution received funding from BioNTech, AltruMed, and Code BioTherapeutics. The remaining authors have disclosed that they do not have any potential conflicts of interest.

Références

Vincent J-L, De Backer D: Circulatory shock. N Engl J Med 2013; 369:1726–1734
Zakkar M, Guida G, Suleiman M-S, et al.: Cardiopulmonary bypass and oxidative stress. Oxid Med Cell Longev 2015; 2015:189863
Raper RF, Cameron G, Walker D, et al.: Type B lactic acidosis following cardiopulmonary bypass. Crit Care Med 1997; 25:46–51
Hu BY, Laine GA, Wang S, et al.: Combined central venous oxygen saturation and lactate as markers of occult hypoperfusion and outcome following cardiac surgery. J Cardiothorac Vasc Anesth 2012; 26:52–57
Hajjar LA, Almeida JP, Fukushima JT, et al.: High lactate levels are predictors of major complications after cardiac surgery. J Thorac Cardiovasc Surg 2013; 146:455–460
Stephens RS, Whitman GJR: Postoperative critical care of the adult cardiac surgical patient. Part I: Routine postoperative care. Crit Care Med 2015; 43:1477–1497
Greenwood JC, Jang DH, Spelde AE, et al.: Low microcirculatory perfused vessel density and high heterogeneity are associated with increased intensity and duration of lactic acidosis after cardiac surgery with cardiopulmonary bypass. Shock 2021; 56:245–254
Greenwood JC, Jang DH, Hallisey SD, et al.: Severe impairment of microcirculatory perfused vessel density is associated with postoperative lactate and acute organ injury after cardiac surgery. J Cardiothorac Vasc Anesth 2021; 35:106–115
Greenwood JC, Talebi FM, Jang DH, et al.: Protocol for the MicroRESUS study: The impact of circulatory shock and resuscitation on microcirculatory function and mitochondrial respiration after cardiovascular surgery. PLoS One 2022; 17:e0273349
Hutchings S, Watts S, Kirkman E: The Cytocam video microscope. A new method for visualising the microcirculation using Incident Dark Field technology. Clin Hemorheol Microcirc 2016; 62:261–271
Ince C, Boerma EC, Cecconi M, et al.; Cardiovascular Dynamics Section of the ESICM: Second consensus on the assessment of sublingual microcirculation in critically ill patients: Results from a task force of the European Society of Intensive Care Medicine. Intensive Care Med 2018; 44:281–299
Massey MJ, Larochelle E, Najarro G, et al.: The microcirculation image quality score: Development and preliminary evaluation of a proposed approach to grading quality of image acquisition for bedside videomicroscopy. J Crit Care 2013; 28:913–917
Li P, Wang B, Sun F, et al.: Mitochondrial respiratory dysfunctions of blood mononuclear cells link with cardiac disturbance in patients with early-stage heart failure. Sci Rep 2015; 5:10229
Jang DH, Orloski CJ, Owiredu S, et al.: Alterations in mitochondrial function in blood cells obtained from patients with sepsis presenting to an emergency department. Shock 2018; 51:580–584
Villarroel JPP, Guan Y, Werlin E, et al.: Hemorrhagic shock and resuscitation are associated with peripheral blood mononuclear cell mitochondrial dysfunction and immunosuppression. J Trauma Acute Care Surg 2013; 75:24–31
Ranucci M, De Toffol B, Isgrò G, et al.: Hyperlactatemia during cardiopulmonary bypass: Determinants and impact on postoperative outcome. Crit Care 2006; 10:R167
Maillet J-M, Le Besnerais P, Cantoni M, et al.: Frequency, risk factors, and outcome of hyperlactatemia after cardiac surgery. Chest 2003; 123:1361–1366
Burša F, Pleva L, Máca J, et al.: Tissue ischemia microdialysis assessments following severe traumatic haemorrhagic shock: Lactate/pyruvate ratio as a new resuscitation end point? BMC Anesthesiol. 2014; 14:118
Rimachi R, Bruzzi de Carvahlo F, Orellano-Jimenez C, et al.: Lactate/pyruvate ratio as a marker of tissue hypoxia in circulatory and septic shock. Anaesth Intensive Care 2012; 40:427–432
Weil MH, Tang W: Forty-five-year evolution of stat blood and plasma lactate measurement to guide critical care. Clin Chem 2009; 55:2053–2054
Totaro RJ, Raper RF: Epinephrine-induced lactic acidosis following cardiopulmonary bypass. Crit Care Med 1997; 25:1693–1699
Edul VSK, Enrico C, Laviolle B, et al.: Quantitative assessment of the microcirculation in healthy volunteers and in patients with septic shock. Crit Care Med 2012; 40:1443–1448
De Backer D, Dubois M-J, Schmartz D, et al.: Microcirculatory alterations in cardiac surgery: Effects of cardiopulmonary bypass and anesthesia. Ann Thorac Surg 2009; 88:1396–1403
Wijntjens GW, Fengler K, Fuernau G, et al.: Prognostic implications of microcirculatory perfusion versus macrocirculatory perfusion in cardiogenic shock: A CULPRIT-SHOCK substudy. Eur Heart J Acute Cardiovasc Care 2019; 9:108–119
Dekker NAM, Veerhoek D, Koning NJ, et al.: Postoperative microcirculatory perfusion and endothelial glycocalyx shedding following cardiac surgery with cardiopulmonary bypass. Anaesthesia 2019; 74:609–618
den Os MM, van den Brom CE, van Leeuwen ALI, et al.: Microcirculatory perfusion disturbances following cardiopulmonary bypass: A systematic review. Crit Care 2020; 24:218
Massey MJ, Hou PC, Filbin M, et al.; ProCESS investigators: Microcirculatory perfusion disturbances in septic shock: Results from the ProCESS trial. Crit Care 2018; 22:308
Hutchings SD, Naumann DN, Hopkins P, et al.: Microcirculatory impairment is associated with multiple organ dysfunction following traumatic hemorrhagic shock: The MICROSHOCK study. Crit Care Med 2018; 46:e889–e896
Pojar M, Mand’ák J, Cibícek N, et al.: Peripheral tissue metabolism during off-pump versus on-pump coronary artery bypass graft surgery: The microdialysis study. Eur J Cardiothorac Surg 2008; 33:899–905
Cherry AD: Mitochondrial dysfunction in cardiac surgery. Anesthesiol Clin 2019; 37:769–785
Brealey D, Brand M, Hargreaves I, et al.: Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 2002; 360:219–223
Solaini G, Harris DA: Biochemical dysfunction in heart mitochondria exposed to ischaemia and reperfusion. Biochem J 2005; 390:377–394
Esteitie N, Hinttala R, Wibom R, et al.: Secondary metabolic effects in complex I deficiency. Ann Neurol 2005; 58:544–552
Weiss SL, Zhang D, Bush J, et al.: Mitochondrial dysfunction is associated with an immune paralysis phenotype in pediatric sepsis. Shock 2020; 54:285–293

Auteurs

John C Greenwood (JC)

Department of Emergency Medicine, Center for Resuscitation Science, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.
Department of Anesthesiology and Critical Care, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

Fatima M Talebi (FM)

Department of Emergency Medicine, Center for Resuscitation Science, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

David H Jang (DH)

Department of Emergency Medicine, Center for Resuscitation Science, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

Audrey E Spelde (AE)

Department of Anesthesiology and Critical Care, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

Emily K Gordon (EK)

Department of Anesthesiology and Critical Care, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

Jiri Horak (J)

Department of Anesthesiology and Critical Care, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

Michael A Acker (MA)

Division of Cardiovascular Surgery, Department of Surgery, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

Todd J Kilbaugh (TJ)

Department of Anesthesiology and Critical Care Medicine, Center for Mitochondrial and Epigenomic Medicine, The Children's Hospital of Philadelphia, Philadelphia, PA.

Frances S Shofer (FS)

Department of Epidemiology & Biostatistics, Department of Emergency Medicine Hospital of the University of Pennsylvania, Philadelphia, PA.

John G T Augoustides (JGT)

Department of Anesthesiology and Critical Care, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

Jacob S Brenner (JS)

Division of Pulmonary, Allergy, & Critical Care, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA.

Vladimir R Muzykantov (VR)

Department of Pharmacology and Center for Translational Targeted Therapeutics and Nanomedicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA.

Jan Bakker (J)

Department of Intensive Care Adults, Erasmus MC University Medical Center, Rotterdam, The Netherlands.

Benjamin S Abella (BS)

Department of Emergency Medicine, Center for Resuscitation Science, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.
Department of Anesthesiology and Critical Care, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA.

Classifications MeSH