Effect of fluid resuscitation on cerebral integrity: A prospective randomised porcine study of haemorrhagic shock.
Journal
European journal of anaesthesiology
ISSN: 1365-2346
Titre abrégé: Eur J Anaesthesiol
Pays: England
ID NLM: 8411711
Informations de publication
Date de publication:
01 Apr 2021
01 Apr 2021
Historique:
pubmed:
6
1
2021
medline:
28
4
2021
entrez:
5
1
2021
Statut:
ppublish
Résumé
The treatment of haemorrhagic shock is a challenging task. Colloids have been regarded as standard treatment, but their safety and benefit have been the subject of controversial debates. Negative effects, including renal failure and increased mortality, have resulted in restrictions on their administration. The cerebral effects of different infusion regimens are largely unknown. The current study investigated the impact of gelatine-polysuccinate, hydroxyethyl starch (HES) and balanced electrolyte solution (BES) on cerebral integrity, focusing on cerebral inflammation, apoptosis and blood flow in pigs. Randomised experimental study. University-affiliated large animal research unit. Twenty-four juvenile pigs aged 8 to 12 weeks. Haemorrhagic shock was induced by controlled arterial blood withdrawal to achieve a combination of relevant blood loss (30 to 40 ml kg-1) and haemodynamic deterioration. After 30 min of shock, fluid resuscitation was started with either gelatine-polysuccinate, HES or BES. The animals were then monitored for 4 h. Cerebral perfusion and diffusion were measured via arterial-spin-labelling MRI. Peripheral tissue perfusion was evaluated via white light spectroscopy. Cortical and hippocampal samples were collected at the end of the experiment. The numbers of cerebral cell nuclei were counted and mRNA expression of markers for cerebral apoptosis [glucose transporter protein type 1 (SLC2A), lipocalin 2 (LCN-2), aquaporin-4 (AQP4)] and inflammation [IL-6, TNF-α, glial fibrillary acidic protein (GFAP)] were determined. The three fluid protocols all stabilised the macrocirculation. Fluid resuscitation significantly increased the cerebral perfusion. Gelatine-polysuccinate and HES initially led to a higher cardiac output but caused haemodilution. Cerebral cell counts (as cells μm-2) were lower after colloid administration in the cortex (gelatine-polysuccinate, 1.8 ± 0.3; HES, 1.9 ± 0.4; each P < 0.05 vs. BES, 2.3 ± 0.2) and the hippocampus (gelatine-polysuccinate, 0.8 ± 0.2; HES, 0.9 ± 0.2; each P < 0.05 vs. BES, 1.1 ± 0.1). After gelatine-polysuccinate, the hippocampal SLC2A and GFAP were lower. After gelatine-polysuccinate, the cortical LCN-2 and TNF-α expression levels were increased (each P < 0.05 vs. BES). In a porcine model, fluid resuscitation by colloids, particularly gelatine-polysuccinate, was associated with the occurrence of cerebral injury. 23 177-07/G 15-1-092; 01/2016.
Sections du résumé
BACKGROUND
BACKGROUND
The treatment of haemorrhagic shock is a challenging task. Colloids have been regarded as standard treatment, but their safety and benefit have been the subject of controversial debates. Negative effects, including renal failure and increased mortality, have resulted in restrictions on their administration. The cerebral effects of different infusion regimens are largely unknown.
OBJECTIVES
OBJECTIVE
The current study investigated the impact of gelatine-polysuccinate, hydroxyethyl starch (HES) and balanced electrolyte solution (BES) on cerebral integrity, focusing on cerebral inflammation, apoptosis and blood flow in pigs.
DESIGN
METHODS
Randomised experimental study.
SETTING
METHODS
University-affiliated large animal research unit.
ANIMALS
METHODS
Twenty-four juvenile pigs aged 8 to 12 weeks.
INTERVENTION
METHODS
Haemorrhagic shock was induced by controlled arterial blood withdrawal to achieve a combination of relevant blood loss (30 to 40 ml kg-1) and haemodynamic deterioration. After 30 min of shock, fluid resuscitation was started with either gelatine-polysuccinate, HES or BES. The animals were then monitored for 4 h.
MAIN OUTCOME MEASURES
METHODS
Cerebral perfusion and diffusion were measured via arterial-spin-labelling MRI. Peripheral tissue perfusion was evaluated via white light spectroscopy. Cortical and hippocampal samples were collected at the end of the experiment. The numbers of cerebral cell nuclei were counted and mRNA expression of markers for cerebral apoptosis [glucose transporter protein type 1 (SLC2A), lipocalin 2 (LCN-2), aquaporin-4 (AQP4)] and inflammation [IL-6, TNF-α, glial fibrillary acidic protein (GFAP)] were determined.
RESULTS
RESULTS
The three fluid protocols all stabilised the macrocirculation. Fluid resuscitation significantly increased the cerebral perfusion. Gelatine-polysuccinate and HES initially led to a higher cardiac output but caused haemodilution. Cerebral cell counts (as cells μm-2) were lower after colloid administration in the cortex (gelatine-polysuccinate, 1.8 ± 0.3; HES, 1.9 ± 0.4; each P < 0.05 vs. BES, 2.3 ± 0.2) and the hippocampus (gelatine-polysuccinate, 0.8 ± 0.2; HES, 0.9 ± 0.2; each P < 0.05 vs. BES, 1.1 ± 0.1). After gelatine-polysuccinate, the hippocampal SLC2A and GFAP were lower. After gelatine-polysuccinate, the cortical LCN-2 and TNF-α expression levels were increased (each P < 0.05 vs. BES).
CONCLUSION
CONCLUSIONS
In a porcine model, fluid resuscitation by colloids, particularly gelatine-polysuccinate, was associated with the occurrence of cerebral injury.
ETHICAL APPROVAL NUMBER
UNASSIGNED
23 177-07/G 15-1-092; 01/2016.
Identifiants
pubmed: 33399378
doi: 10.1097/EJA.0000000000001416
pii: 00003643-202104000-00012
doi:
Substances chimiques
Hydroxyethyl Starch Derivatives
0
Types de publication
Journal Article
Randomized Controlled Trial
Langues
eng
Sous-ensembles de citation
IM
Pagination
411-421Informations de copyright
Copyright © 2021 European Society of Anaesthesiology and Intensive Care. Unauthorized reproduction of this article is prohibited.
Références
Kutcher ME, Kornblith LZ, Narayan R, et al. A paradigm shift in trauma resuscitation: evaluation of evolving massive transfusion practices. JAMA Surg 2013; 148:834–840.
Noll E, Diana M, Charles AL, et al. Comparative analysis of resuscitation using human serum albumin and crystalloids or 130/0.4 hydroxyethyl starch and crystalloids on skeletal muscle metabolic profile during experimental haemorrhagic shock in swine: a randomised experimental study. Eur J Anaesthesiol 2017; 34:89–97.
Oller L, Dyer WB, Santamaria L, et al. The effect of a novel intravenous fluid (Oxsealife(R)) on recovery from haemorrhagic shock in pigs. Anaesthesia 2019; 74:765–777.
Kerger H, Waschke KF, Ackern KV, et al. Systemic and microcirculatory effects of autologous whole blood resuscitation in severe hemorrhagic shock. Am J Physiol 1999; 276:H2035–H2043.
Siegemund M, Hollinger A, Gebhard EC, et al. The value of volume substitution in patients with septic and haemorrhagic shock with respect to the microcirculation. Swiss Med Wkly 2019; 149:w20007.
Spahn DR, Bouillon B, Cerny V, et al. The European guideline on management of major bleeding and coagulopathy following trauma: fifth edition. Crit Care 2019; 23:98.
Guidet B, Martinet O, Boulain T, et al. Assessment of hemodynamic efficacy and safety of 6% hydroxyethylstarch 130/0.4 vs. 0.9% NaCl fluid replacement in patients with severe sepsis: the CRYSTMAS study. Crit Care 2012; 16:R94.
Brunkhorst FM, Engel C, Bloos F, et al. Intensive insulin therapy and pentastarch resuscitation in severe sepsis. N Engl J Med 2008; 358:125–139.
Perner A, Haase N, Guttormsen AB, et al. Hydroxyethyl starch 130/0.42 versus Ringer's acetate in severe sepsis. N Engl J Med 2012; 367:124–134.
Annane D, Siami S, Jaber S, et al. Effects of fluid resuscitation with colloids vs crystalloids on mortality in critically ill patients presenting with hypovolemic shock: the CRISTAL randomized trial. JAMA 2013; 310:1809–1817.
Dellinger RP, Levy MM, Rhodes A, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock, 2012. Intensive Care Med 2013; 39:165–228.
Myburgh JA, Finfer S, Bellomo R, et al. Hydroxyethyl starch or saline for fluid resuscitation in intensive care. N Engl J Med 2012; 367:1901–1911.
Zaar M, Lauritzen B, Secher NH, et al. Initial administration of hydroxyethyl starch vs lactated Ringer after liver trauma in the pig. Br J Anaesth 2009; 102:221–226.
Mauch J, Madjdpour C, Kutter AP, et al. Effect of rapid fluid resuscitation using crystalloids or colloids on hemostasis in piglets. Paediatr Anaesth 2013; 23:258–264.
Laake JH, Tonnessen TI, Chew MS, et al. The SSAI fully supports the suspension of hydroxyethyl-starch solutions commissioned by the European Medicines Agency. Acta Anaesthesiol Scand 2018; 62:874–875.
Rehm M, Hulde N, Kammerer T, et al. State of the art in fluid and volume therapy: a user-friendly staged concept. English version. Anaesthesist 2019; 68: (Suppl 1): 1–14.
Ziebart A, Möllmann C, Garcia-Bardon A, et al. Effect of gelatin-polysuccinat on cerebral oxygenation and microcirculation in a porcine haemorrhagic shock model. Scand J Trauma Resusc Emerg Med 2018; 26:15.
Adamik KN, Yozova ID. Starch Wars – new episodes of the Saga. Changes in regulations on hydroxyethyl starch in the European Union. Front Vet Sci 2018; 5:336.
Moeller C, Fleischmann C, Thomas-Rueddel D, et al. How safe is gelatin? A systematic review and meta-analysis of gelatin-containing plasma expanders vs crystalloids and albumin. J Crit Care 2016; 35:75–83.
Awad S, Dharmavaram S, Wearn CS, et al. Effects of an intraoperative infusion of 4% succinylated gelatine (Gelofusine(R)) and 6% hydroxyethyl starch (Voluven(R)) on blood volume. Br J Anaesth 2012; 109:168–176.
Qureshi SH, Rizvi SI, Patel NN, et al. Meta-analysis of colloids versus crystalloids in critically ill, trauma and surgical patients. Br J Surg 2016; 103:14–26.
Wu CY, Chan KC, Cheng YJ, et al. Effects of different types of fluid resuscitation for hemorrhagic shock on splanchnic organ microcirculation and renal reactive oxygen species formation. Crit Care 2015; 19:434.
Hippensteel JA, Uchimido R, Tyler PD, et al. Intravenous fluid resuscitation is associated with septic endothelial glycocalyx degradation. Crit Care 2019; 23:259.
Dekker SE, Sillesen M, Bambakidis T, et al. Normal saline influences coagulation and endothelial function after traumatic brain injury and hemorrhagic shock in pigs. Surgery 2014; 156:556–563.
Ziebart A, Kamuf J, Ruemmler R, et al. Standardized hemorrhagic shock induction guided by cerebral oximetry and extended hemodynamic monitoring in pigs. J Vis Exp 2019; doi: 10.3791/59332.
doi: 10.3791/59332
Ziebart A, Ruemmler R, Möllmann C, et al. Fluid resuscitation-related coagulation impairment in a porcine hemorrhagic shock model. PeerJ 2020; 8:e8399.
Ha JY, Choi YH, Lee S, et al. Arterial spin labeling MRI for quantitative assessment of cerebral perfusion before and after cerebral revascularization in children with moyamoya disease. Korean J Radiol 2019; 20:985–996.
Bock M. Magnetic resonance angiography without contrast agents. Radiologe 2019; 59:523–532.
Detre JA, Rao H, Wang DJ, et al. Applications of arterial spin labeled MRI in the brain. J Magn Reson Imaging 2012; 35:1026–1037.
Ziebart A, Schaefer MM, Thomas R, et al. Random allogeneic blood transfusion in pigs: characterisation of a novel experimental model. PeerJ 2019; 7:e7439.
Noll E, Diana M, Charles AL, et al. Comparative analysis of resuscitation using human serum albumin and crystalloids or 130/0.4 hydroxyethyl starch and crystalloids on skeletal muscle metabolic profile during experimental haemorrhagic shock in swine: a randomised experimental study. Eur J Anaesth 2017; 34:89–97.
Witt L, Glage S, Lichtinghagen R, et al. Impact of high doses of 6% hydroxyethyl starch 130/0.42 and 4% gelatin on renal function in a pediatric animal model. Paediatr Anaesth 2016; 26:259–265.
Selmaj K, Shafit-Zagardo B, Aquino DA, et al. Tumor necrosis factor-induced proliferation of astrocytes from mature brain is associated with down-regulation of glial fibrillary acidic protein mRNA. J Neurochem 1991; 57:823–830.
Mueckler M, Thorens B. The SLC2 (GLUT) family of membrane transporters. Mol Aspects Med 2013; 34:121–138.
Russo VC, Kobayashi K, Najdovska S, et al. Neuronal protection from glucose deprivation via modulation of glucose transport and inhibition of apoptosis: a role for the insulin-like growth factor system. Brain Res 2004; 1009:40–53.
Suk K. Lipocalin-2 as a therapeutic target for brain injury: an astrocentric perspective. Prog Neurobiol 2016; 144:158–172.
Guiddir T, Deghmane AE, Giorgini D, et al. Lipocalin 2 in cerebrospinal fluid as a marker of acute bacterial meningitis. BMC Infect Dis 2014; 14:276.
Wang G, Weng YC, Han X, et al. Lipocalin-2 released in response to cerebral ischaemia mediates reperfusion injury in mice. J Cell Mol Med 2015; 19:1637–1645.
Silverman HA, Dancho M, Regnier-Golanov A, et al. Brain region-specific alterations in the gene expression of cytokines, immune cell markers and cholinergic system components during peripheral endotoxin-induced inflammation. Mol Med 2015; 20:601–611.
Wahul AB, Joshi PC, Kumar A, et al. Transient global cerebral ischemia differentially affects cortex, striatum and hippocampus in Bilateral Common Carotid Arterial occlusion (BCCAo) mouse model. J Chem Neuroanat 2018; 92:1–15.
Xu H, Lu A, Sharp FR. Regional genome transcriptional response of adult mouse brain to hypoxia. BMC Genomics 2011; 12:499.
Orbegozo Cortes D, Gamarano Barros T, Njimi H, et al. Crystalloids versus colloids: exploring differences in fluid requirements by systematic review and meta-regression. Anesth Analg 2015; 120:389–402.
Yao FS, Tseng CC, Ho CY, et al. Cerebral oxygen desaturation is associated with early postoperative neuropsychological dysfunction in patients undergoing cardiac surgery. J Cardiothorac Vasc Anesth 2004; 18:552–558.
Brodt J, Vladinov G, Castillo-Pedraza C, et al. Changes in cerebral oxygen saturation during transcatheter aortic valve replacement. J Clin Monit Comput 2016; 30:649–653.
Fan FC, Chen RY, Schuessler GB, et al. Effects of hematocrit variations on regional hemodynamics and oxygen transport in the dog. Am J Physiol 1980; 238:H545–H622.
Crystal GJ, Czinn EA, Salem MR. The mechanism of increased blood flow in the brain and spinal cord during hemodilution. Anesth Analg 2014; 118:637–643.
Doblinger N, Bredthauer A, Mohrez M, et al. Impact of hydroxyethyl starch and modified fluid gelatin on granulocyte phenotype and function. Transfusion 2019; 59:2121–2130.
Albrecht FW, Glas M, Rensing H, et al. A change of colloid from hydroxyethyl starch to gelatin does not reduce rate of renal failure or mortality in surgical critical care patients: results of a retrospective cohort study. J Crit Care 2016; 36:160–165.
Pisano A, Landoni G, Bellomo R. The risk of infusing gelatin? Die-hard misconceptions and forgotten (or ignored) truths. Minerva Anestesiol 2016; 82:1107–1114.
Krabbe J, Ruske N, Braunschweig T, et al. The effects of hydroxyethyl starch and gelatine on pulmonary cytokine production and oedema formation. Sci Rep 2018; 8:5123.
Öztürk T, Onur E, Cerrahoğlu M, et al. Immune and inflammatory role of hydroxyethyl starch 130/0.4 and fluid gelatin in patients undergoing coronary surgery. Cytokine 2015; 74:69–75.
Smart L, Boyd CJ, Claus MA, et al. Large-volume crystalloid fluid is associated with increased hyaluronan shedding and inflammation in a canine hemorrhagic shock model. Inflammation 2018; 41:1515–1523.
Zhu J, Li X, Yin J, et al. Glycocalyx degradation leads to blood-brain barrier dysfunction and brain edema after asphyxia cardiac arrest in rats. J Cereb Blood Flow Metab 2018; 38:1979–1992.
Ziebart A, Hartmann EK, Thomas R, et al. Low tidal volume pressure support versus controlled ventilation in early experimental sepsis in pigs. Respir Res 2014; 15:101.