Recovery of organ-specific tissue oxygen delivery at restrictive transfusion thresholds after fluid treatment in ovine haemorrhagic shock.
Haemodilution
Haemorrhagic shock
Microcirculation
Oxygen debt
Patient blood management
Tissue oxygen delivery
Transfusion thresholds
Journal
Intensive care medicine experimental
ISSN: 2197-425X
Titre abrégé: Intensive Care Med Exp
Pays: Germany
ID NLM: 101645149
Informations de publication
Date de publication:
04 Apr 2022
04 Apr 2022
Historique:
received:
17
01
2022
accepted:
20
03
2022
entrez:
4
4
2022
pubmed:
5
4
2022
medline:
5
4
2022
Statut:
epublish
Résumé
Fluid resuscitation is the standard treatment to restore circulating blood volume and pressure after massive haemorrhage and shock. Packed red blood cells (PRBC) are transfused to restore haemoglobin levels. Restoration of microcirculatory flow and tissue oxygen delivery is critical for organ and patient survival, but these parameters are infrequently measured. Patient Blood Management is a multidisciplinary approach to manage and conserve a patient's own blood, directing treatment options based on broad clinical assessment beyond haemoglobin alone, for which tissue perfusion and oxygenation could be useful. Our aim was to assess utility of non-invasive tissue-specific measures to compare PRBC transfusion with novel crystalloid treatments for haemorrhagic shock. A model of severe haemorrhagic shock was developed in an intensive care setting, with controlled haemorrhage in sheep according to pressure (mean arterial pressure 30-40 mmHg) and oxygen debt (lactate > 4 mM) targets. We compared PRBC transfusion to fluid resuscitation with either PlasmaLyte or a novel crystalloid. Efficacy was assessed according to recovery of haemodynamic parameters and non-invasive measures of sublingual microcirculatory flow, regional tissue oxygen saturation, repayment of oxygen debt (arterial lactate), and a panel of inflammatory and organ function markers. Invasive measurements of tissue perfusion, oxygen tension and lactate levels were performed in brain, kidney, liver, and skeletal muscle. Outcomes were assessed during 4 h treatment and post-mortem, and analysed by one- and two-way ANOVA. Each treatment restored haemodynamic and tissue oxygen delivery parameters equivalently (p > 0.05), despite haemodilution after crystalloid infusion to haemoglobin concentrations below 70 g/L (p < 0.001). Recovery of vital organ-specific perfusion and oxygen tension commenced shortly before non-invasive measures improved. Lactate declined in all tissues and correlated with arterial lactate levels (p < 0.0001). The novel crystalloid supported rapid peripheral vasodilation (p = 0.014) and tended to achieve tissue oxygen delivery targets earlier. PRBC supported earlier renal oxygen delivery (p = 0.012) but delayed peripheral perfusion (p = 0.034). Crystalloids supported vital organ oxygen delivery after massive haemorrhage, despite haemodilution to < 70 g/L, confirming that restrictive transfusion thresholds are appropriate to support oxygen delivery. Non-invasive tissue perfusion and oximetry technologies merit further clinical appraisal to guide treatment for massive haemorrhage in the context of Patient Blood Management.
Sections du résumé
BACKGROUND
BACKGROUND
Fluid resuscitation is the standard treatment to restore circulating blood volume and pressure after massive haemorrhage and shock. Packed red blood cells (PRBC) are transfused to restore haemoglobin levels. Restoration of microcirculatory flow and tissue oxygen delivery is critical for organ and patient survival, but these parameters are infrequently measured. Patient Blood Management is a multidisciplinary approach to manage and conserve a patient's own blood, directing treatment options based on broad clinical assessment beyond haemoglobin alone, for which tissue perfusion and oxygenation could be useful. Our aim was to assess utility of non-invasive tissue-specific measures to compare PRBC transfusion with novel crystalloid treatments for haemorrhagic shock.
METHODS
METHODS
A model of severe haemorrhagic shock was developed in an intensive care setting, with controlled haemorrhage in sheep according to pressure (mean arterial pressure 30-40 mmHg) and oxygen debt (lactate > 4 mM) targets. We compared PRBC transfusion to fluid resuscitation with either PlasmaLyte or a novel crystalloid. Efficacy was assessed according to recovery of haemodynamic parameters and non-invasive measures of sublingual microcirculatory flow, regional tissue oxygen saturation, repayment of oxygen debt (arterial lactate), and a panel of inflammatory and organ function markers. Invasive measurements of tissue perfusion, oxygen tension and lactate levels were performed in brain, kidney, liver, and skeletal muscle. Outcomes were assessed during 4 h treatment and post-mortem, and analysed by one- and two-way ANOVA.
RESULTS
RESULTS
Each treatment restored haemodynamic and tissue oxygen delivery parameters equivalently (p > 0.05), despite haemodilution after crystalloid infusion to haemoglobin concentrations below 70 g/L (p < 0.001). Recovery of vital organ-specific perfusion and oxygen tension commenced shortly before non-invasive measures improved. Lactate declined in all tissues and correlated with arterial lactate levels (p < 0.0001). The novel crystalloid supported rapid peripheral vasodilation (p = 0.014) and tended to achieve tissue oxygen delivery targets earlier. PRBC supported earlier renal oxygen delivery (p = 0.012) but delayed peripheral perfusion (p = 0.034).
CONCLUSIONS
CONCLUSIONS
Crystalloids supported vital organ oxygen delivery after massive haemorrhage, despite haemodilution to < 70 g/L, confirming that restrictive transfusion thresholds are appropriate to support oxygen delivery. Non-invasive tissue perfusion and oximetry technologies merit further clinical appraisal to guide treatment for massive haemorrhage in the context of Patient Blood Management.
Identifiants
pubmed: 35377109
doi: 10.1186/s40635-022-00439-6
pii: 10.1186/s40635-022-00439-6
pmc: PMC8980119
doi:
Types de publication
Journal Article
Langues
eng
Pagination
12Subventions
Organisme : National Blood Authority
ID : ID316
Informations de copyright
© 2022. The Author(s).
Références
Lozano R, Naghavi M, Foreman K et al (2012) Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380(9859):2095–2128
pubmed: 23245604
Siegemund M, Hollinger A, Gebhard EC et al (2019) The value of volume substitution in patients with septic and haemorrhagic shock with respect to the microcirculation. Swiss Med Wkly 149:w20007
pubmed: 30715722
Jiang LM, He J, Xi XY et al (2019) Effect of early restrictive fluid resuscitation on inflammatory and immune factors in patients with severe pelvic fracture. Chin J Traumatol 22(6):311–315
pubmed: 31685356
pmcid: 6923289
Tran A, Yates J, Lau A et al (2018) Permissive hypotension versus conventional resuscitation strategies in adult trauma patients with hemorrhagic shock: a systematic review and meta-analysis of randomized controlled trials. J Trauma Acute Care Surg 84(5):802–808
pubmed: 29370058
Moreno DH, Cacione DG, Baptista-Silva JC (2018) Controlled hypotension versus normotensive resuscitation strategy for people with ruptured abdominal aortic aneurysm. Cochrane Database Syst Rev 6(6):CD011664
pubmed: 29897100
Stein P, Kaserer A, Sprengel K et al (2017) Change of transfusion and treatment paradigm in major trauma patients. Anaesthesia 72(11):1317–1326
pubmed: 28542848
Winearls J, Campbell D, Hurn C et al (2017) Fibrinogen in traumatic haemorrhage: a narrative review. Injury 48(2):230–242
pubmed: 28088374
van Turenhout EC, Bossers SM, Loer SA et al (2020) Pre-hospital transfusion of red blood cells. Part 2: A systematic review of treatment effects on outcomes. Transfus Med 30(2):106–133
pubmed: 31903684
pmcid: 7317762
Cantle PM, Cotton BA (2017) Balanced resuscitation in trauma management. Surg Clin North Am 97(5):999–1014
pubmed: 28958369
Shea SM, Staudt AM, Thomas KA et al (2020) The use of low-titer group O whole blood is independently associated with improved survival compared to component therapy in adults with severe traumatic hemorrhage. Transfusion 60(Suppl 3):S2-s9
pubmed: 32478896
Rehn M, Weaver AE, Eshelby S et al (2018) Pre-hospital transfusion of red blood cells in civilian trauma patients. Transfus Med 28(4):277–283
pubmed: 29067785
Napolitano LM, Kurek S, Luchette FA et al (2009) Clinical practice guideline: red blood cell transfusion in adult trauma and critical care. Crit Care Med 37(12):3124–3157
pubmed: 19773646
Derzon JH, Clarke N, Alford A et al (2019) Restrictive transfusion strategy and clinical decision support practices for reducing RBC transfusion overuse. Am J Clin Pathol 152(5):544–557
pubmed: 31305890
National Blood Authority. Patient Blood Management Guidelines: Module 2 Perioperative. Canberra, ACT, Australia.2012. Available from: https://www.blood.gov.au/pbm-module-2 . Accessed Sept 2021
Whitlock EL, Kim H, Auerbach AD (2015) Harms associated with single unit perioperative transfusion: retrospective population based analysis. BMJ 350:h3037
pubmed: 26070979
pmcid: 4463965
Shander A, Javidroozi M, Ozawa S et al (2011) What is really dangerous: anaemia or transfusion? Br J Anaesth 107(Suppl 1):i41-59
pubmed: 22156270
Salpeter SR, Buckley JS, Chatterjee S (2014) Impact of more restrictive blood transfusion strategies on clinical outcomes: a meta-analysis and systematic review. Am J Med 127(2):124–31.e3
pubmed: 24331453
Scheuzger J, Zehnder A, Meier V et al (2020) Sublingual microcirculation does not reflect red blood cell transfusion thresholds in the intensive care unit-a prospective observational study in the intensive care unit. Crit Care 24(1):18
pubmed: 31952555
pmcid: 6969438
Tsai AG, Friesenecker B, Intaglietta M (1995) Capillary flow impairment and functional capillary density. Int J Microcirc Clin Exp 15(5):238–243
pubmed: 8852621
Benni PB, MacLeod D, Ikeda K et al (2018) A validation method for near-infrared spectroscopy based tissue oximeters for cerebral and somatic tissue oxygen saturation measurements. J Clin Monit Comput 32(2):269–284
pubmed: 28374103
Bjerkvig CK, Strandenes G, Eliassen HS et al (2016) “Blood failure” time to view blood as an organ: how oxygen debt contributes to blood failure and its implications for remote damage control resuscitation. Transfusion 56(Suppl 2):S182–S189
pubmed: 27100755
Spahn DR, Bouillon B, Cerny V et al (2019) The European guideline on management of major bleeding and coagulopathy following trauma: fifth edition. Crit Care 23(1):98
pubmed: 30917843
pmcid: 6436241
Cole E, Weaver A, Gall L et al (2019) A decade of damage control resuscitation: new transfusion practice, new survivors, new directions. Ann Surg 273:1215
Goobie SM, Shander A (2020) One size does not fit all in treating massive hemorrhage. Anesth Analg 131(2):480–482
pubmed: 32665498
Weinberg L, Collins N, Van Mourik K et al (2016) Plasma-Lyte 148: a clinical review. World J Crit Care Med 5(4):235–250
pubmed: 27896148
pmcid: 5109922
Oller Duque L, Shander A (2018) Isotonic Crystalloid Aqueous Solution. World Intellectual Property Organization. WO/2018/019663
Oller L, Dyer WB, Santamaría L et al (2019) The effect of a novel intravenous fluid (Oxsealife
pubmed: 30920660
Dyer WB, Tung JP, Li Bassi G et al (2021) An ovine model of haemorrhagic shock and resuscitation, to assess recovery of tissue oxygen delivery and oxygen debt, and inform Patient Blood Management. Shock 56(6):1080–1091
pubmed: 34014886
Perry M (1998) Revised Australian code of practice for the care and use of animals for scientific purposes. Aust Vet J 76(4):286
pubmed: 9612553
Simonova G, Tung JP, Fraser JF et al (2014) A comprehensive ovine model of blood transfusion. Vox Sang 106(2):153–160
pubmed: 23992472
Chemonges S, Shekar K, Tung JP et al (2014) Optimal management of the critically ill: anaesthesia, monitoring, data capture, and point-of-care technological practices in ovine models of critical care. Biomed Res Int 2014:468309
pubmed: 24783206
pmcid: 3982457
Wilson DV, Evans AT, Carpenter RA et al (2004) The effect of four anesthetic protocols on splenic size in dogs. Vet Anaesth Analg 31(2):102–108
pubmed: 15053748
Musk GC, Kershaw H, Kemp MW (2019) Anaemia and hypoproteinaemia in pregnant sheep during anaesthesia. Animals 9(4):156
pmcid: 6523546
Dooley PC, Hecker JF, Webster ME (1972) Contraction of the sheep’s spleen. Aust J Exp Biol Med Sci 50(6):745–755
pubmed: 4656788
Hodgetts VE (1961) The dynamic red cell storage function of the spleen in sheep. III. Relationship to determination of blood volume, total red cell volume, and plasma volume. Aust J Exp Biol Med Sci 39:187–195
pubmed: 13714848
Foley SR, Solano C, Simonova G et al (2014) A comprehensive study of ovine haemostasis to assess suitability to model human coagulation. Thromb Res 134(2):468–473
pubmed: 24929837
Bouquet M, Passmore MR, See Hoe LE et al (2020) Development and validation of ELISAs for the quantitation of interleukin (IL)-1β, IL-6, IL-8 and IL-10 in ovine plasma. J Immunol Methods 486:112835
pubmed: 32828792
Julien M, Flick MR, Hoeffel JM et al (1984) Accurate reference measurement for postmortem lung water. J Appl Physiol Respir Environ Exerc Physiol 56(1):248–253
pubmed: 6693329
Shander A, Javidroozi M, Naqvi S et al (2014) An update on mortality and morbidity in patients with very low postoperative hemoglobin levels who decline blood transfusion (CME). Transfusion 54(10 Pt 2):2688–2695
pubmed: 24527739
Hong T, Shander A, Agarwal S et al (2015) Management of a Jehovah’s witness patient with sepsis and profuse bleeding after emergency coronary artery bypass graft surgery: rethinking the critical threshold of oxygen delivery. A A Case Rep 4(10):127–131
pubmed: 25974416
Saugel B, Klein M, Hapfelmeier A et al (2013) Effects of red blood cell transfusion on hemodynamic parameters: a prospective study in intensive care unit patients. Scand J Trauma Resusc Emerg Med 21:21
pubmed: 23531382
pmcid: 3620943
Manning RD Jr, Guyton AC (1983) Effects of hypoproteinemia on fluid volumes and arterial pressure. Am J Physiol 245(2):H284–H293
pubmed: 6881362
Wu F, Chipman A, Pati S et al (2020) Resuscitative strategies to modulate the endotheliopathy of trauma: from cell to patient. Shock 53(5):575–584
pubmed: 31090680
pmcid: 6842415
Halbgebauer R, Braun CK, Denk S et al (2018) Hemorrhagic shock drives glycocalyx, barrier and organ dysfunction early after polytrauma. J Crit Care 44:229–237
pubmed: 29175047
Ergin B, van Rooij T, Lima A et al (2021) Hydroxyl Ethyl Starch (HES) preserves intrarenal microcirculatory perfusion shown by contrast-enhanced ultrasound (CEUS), and renal function in a severe hemodilution model in pigs. Shock 57:457
Cabrales P, Intaglietta M, Tsai AG (2007) Transfusion restores blood viscosity and reinstates microvascular conditions from hemorrhagic shock independent of oxygen carrying capacity. Resuscitation 75(1):124–134
pubmed: 17481796
pmcid: 3224809
Quinton R (1912) L'eau de Mer; Meileu Organique. Editor: Masson. https://openlibrary.org/books/OL24240755M/L%27eau_de_mer_milieu_organique . Accessed 5 Nov 2021
Tsai AG, Vazquez BY, Hofmann A et al (2015) Supra-plasma expanders: the future of treating blood loss and anemia without red cell transfusions? J Infus Nurs 38(3):217–222
pubmed: 25871869
pmcid: 5608479
Villela NR, Salazar Vazquez BY, Intaglietta M (2009) Microcirculatory effects of intravenous fluids in critical illness: plasma expansion beyond crystalloids and colloids. Curr Opin Anaesthesiol 22(2):163–167
pubmed: 19307891
Davie SN, Grocott HP (2012) Impact of extracranial contamination on regional cerebral oxygen saturation: a comparison of three cerebral oximetry technologies. Anesthesiology 116(4):834–840
pubmed: 22343469
Greenberg S, Murphy G, Shear T et al (2016) Extracranial contamination in the INVOS 5100C versus the FORE-SIGHT ELITE cerebral oximeter: a prospective observational crossover study in volunteers. Can J Anaesth 63(1):24–30
pubmed: 26307186
Dixon B, MacLeod DB (2020) Assessment of a non invasive brain oximeter in volunteers undergoing acute hypoxia. Med Devices 13:183–194
Lange F, Bale G, Kaynezhad P et al (2020) Broadband NIRS cerebral evaluation of the hemodynamic and oxidative state of cytochrome-c-oxidase responses to +Gz acceleration in healthy volunteers. Adv Exp Med Biol 1232:339–345
pubmed: 31893429
Mik EG, Balestra GM, Harms FA (2020) Monitoring mitochondrial PO2: the next step. Curr Opin Crit Care 26(3):289–295
pubmed: 32348095
Messina A, Robba C, Calabrò L et al (2021) Association between perioperative fluid administration and postoperative outcomes: a 20-year systematic review and a meta-analysis of randomized goal-directed trials in major visceral/noncardiac surgery. Crit Care 25(1):43
pubmed: 33522953
pmcid: 7849093
Ramesh GH, Uma JC, Farhath S (2019) Fluid resuscitation in trauma: what are the best strategies and fluids? Int J Emerg Med 12(1):38
pubmed: 31801458
pmcid: 6894336