The Effects of Temperature Management on Brain Microcirculation, Oxygenation and Metabolism

Overview

Journal Brain Sci

Publisher MDPI

Date 2022 Oct 27

PMID 36291355

Authors

Katia Donadello

Fuhong Su

Filippo Annoni

Sabino Scolletta

Xinrong He

Lorenzo Peluso

Leonardo Gottin

Enrico Polati

Jacques Creteur

Olivier De Witte

Jean-Louis Vincent

Daniel De Backer

Fabio Silvio Taccone

Affiliations

Soon will be listed here.

Abstract

Purpose: Target temperature management (TTM) is often used in patients after cardiac arrest, but the effects of cooling on cerebral microcirculation, oxygenation and metabolism are poorly understood. We studied the time course of these variables in a healthy swine model.

Methods: Fifteen invasively monitored, mechanically ventilated pigs were allocated to sham procedure (normothermia, NT; = 5), cooling (hypothermia, HT, = 5) or cooling with controlled oxygenation (HT-Oxy, = 5). Cooling was induced by cold intravenous saline infusion, ice packs and nasal cooling to achieve a body temperature of 33-35 °C. After 6 h, animals were rewarmed to baseline temperature (within 5 h). The cerebral microvascular network was evaluated (at baseline and 2, 7 and 12 h thereafter) using sidestream dark-field (SDF) video-microscopy. Cerebral blood flow (laser Doppler MNP100XP, Oxyflow, Oxford Optronix, Oxford, UK), oxygenation (PbtO, Licox catheter, Integra Lifesciences, USA) and lactate/pyruvate ratio (LPR) using brain microdialysis (CMA, Stockholm, Sweden) were measured hourly.

Results: In HT animals, cerebral functional capillary density (FCD) and proportion of small-perfused vessels (PSPV) significantly decreased over time during the cooling phase; concomitantly, PbtO increased and LPR decreased. After rewarming, all microcirculatory variables returned to normal values, except LPR, which increased during the rewarming phase in the two groups subjected to HT when compared to the group maintained at normothermia.

Conclusions: In healthy animals, TTM can be associated with alterations in cerebral microcirculation during cooling and altered metabolism at rewarming.

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References

De Backer D, Ortiz J, Salgado D . Coupling microcirculation to systemic hemodynamics. Curr Opin Crit Care. 2010; 16(3):250-4. DOI: 10.1097/MCC.0b013e3283383621. View

Chu D, Kim L, Young P, Zamiri N, Almenawer S, Jaeschke R . Mortality and morbidity in acutely ill adults treated with liberal versus conservative oxygen therapy (IOTA): a systematic review and meta-analysis. Lancet. 2018; 391(10131):1693-1705. DOI: 10.1016/S0140-6736(18)30479-3. View

Kurz A, Sessler D, Lenhardt R . Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. Study of Wound Infection and Temperature Group. N Engl J Med. 1996; 334(19):1209-15. DOI: 10.1056/NEJM199605093341901. View

Hollyer T, Bordoni L, Kousholt B, Van Luijk J, Ritskes-Hoitinga M, Ostergaard L . The evidence for the physiological effects of lactate on the cerebral microcirculation: a systematic review. J Neurochem. 2018; 148(6):712-730. PMC: 6590437. DOI: 10.1111/jnc.14633. View

Larach D, Kofke W, le Roux P . Potential non-hypoxic/ischemic causes of increased cerebral interstitial fluid lactate/pyruvate ratio: a review of available literature. Neurocrit Care. 2011; 15(3):609-22. DOI: 10.1007/s12028-011-9517-8. View

Tsai A, Cabrales P, Winslow R, Intaglietta M . Microvascular oxygen distribution in awake hamster window chamber model during hyperoxia. Am J Physiol Heart Circ Physiol. 2003; 285(4):H1537-45. DOI: 10.1152/ajpheart.00176.2003. View

Panerai R . Assessment of cerebral pressure autoregulation in humans--a review of measurement methods. Physiol Meas. 1998; 19(3):305-38. DOI: 10.1088/0967-3334/19/3/001. View

Casamento A, Minson A, Radford S, Martensson J, Ridgeon E, Young P . A comparison of therapeutic hypothermia and strict therapeutic normothermia after cardiac arrest. Resuscitation. 2016; 106:83-8. DOI: 10.1016/j.resuscitation.2016.06.019. View

Boerma E, van der Voort P, Spronk P, Ince C . Relationship between sublingual and intestinal microcirculatory perfusion in patients with abdominal sepsis. Crit Care Med. 2007; 35(4):1055-60. DOI: 10.1097/01.CCM.0000259527.89927.F9. View

10.

Timofeev I, Czosnyka M, Carpenter K, Nortje J, Kirkpatrick P, Al-Rawi P . Interaction between brain chemistry and physiology after traumatic brain injury: impact of autoregulation and microdialysis catheter location. J Neurotrauma. 2011; 28(6):849-60. PMC: 3113421. DOI: 10.1089/neu.2010.1656. View

11.

Marion D, Penrod L, Kelsey S, Obrist W, Kochanek P, Palmer A . Treatment of traumatic brain injury with moderate hypothermia. N Engl J Med. 1997; 336(8):540-6. DOI: 10.1056/NEJM199702203360803. View

12.

Taccone F, Su F, De Deyne C, Abdellhai A, Pierrakos C, He X . Sepsis is associated with altered cerebral microcirculation and tissue hypoxia in experimental peritonitis. Crit Care Med. 2013; 42(2):e114-22. DOI: 10.1097/CCM.0b013e3182a641b8. View

13.

Young P, Mackle D, Bellomo R, Bailey M, Beasley R, Deane A . Conservative oxygen therapy for mechanically ventilated adults with suspected hypoxic ischaemic encephalopathy. Intensive Care Med. 2020; 46(12):2411-2422. PMC: 7431900. DOI: 10.1007/s00134-020-06196-y. View

14.

Donadello K, Favory R, Salgado-Ribeiro D, Vincent J, Gottin L, Scolletta S . Sublingual and muscular microcirculatory alterations after cardiac arrest: a pilot study. Resuscitation. 2011; 82(6):690-5. DOI: 10.1016/j.resuscitation.2011.02.018. View

15.

Kamler M, Wendt D, Pizanis N, Milekhin V, Schade U, Jakob H . Deleterious effects of oxygen during extracorporeal circulation for the microcirculation in vivo. Eur J Cardiothorac Surg. 2004; 26(3):564-70. DOI: 10.1016/j.ejcts.2004.05.045. View

16.

Bakker J, Coffernils M, Leon M, Gris P, Vincent J . Blood lactate levels are superior to oxygen-derived variables in predicting outcome in human septic shock. Chest. 1991; 99(4):956-62. DOI: 10.1378/chest.99.4.956. View

17.

Chierego M, Verdant C, De Backer D . Microcirculatory alterations in critically ill patients. Minerva Anestesiol. 2006; 72(4):199-205. View

18.

Bernard S, Gray T, Buist M, Jones B, Silvester W, Gutteridge G . Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med. 2002; 346(8):557-63. DOI: 10.1056/NEJMoa003289. View

19.

Nielsen N, Wetterslev J, Cronberg T, Erlinge D, Gasche Y, Hassager C . Targeted temperature management at 33°C versus 36°C after cardiac arrest. N Engl J Med. 2013; 369(23):2197-206. DOI: 10.1056/NEJMoa1310519. View

20.

Magnoni S, Ghisoni L, Locatelli M, Caimi M, Colombo A, Valeriani V . Lack of improvement in cerebral metabolism after hyperoxia in severe head injury: a microdialysis study. J Neurosurg. 2003; 98(5):952-8. DOI: 10.3171/jns.2003.98.5.0952. View