Cerebral metabolic effects of exogenous lactate supplementation on the injured human brain

Intensive Care Medicine

Volumn 40, Issue 3, 2014, Pages 412-421

  Bouzat, Pierre ^a,b   Sala, Nathalie ^a   Suys, Tamarah ^a   Zerlauth, Jean Baptiste ^a   Marques Vidal, Pedro ^c   Feihl, François ^a   Bloch, Jocelyne ^a   Messerer, Mahmoud ^a   Levivier, Marc ^a   Meuli, Reto ^a   Magistretti, Pierre J ^a   Oddo, Mauro ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIV GRENOBLE ALPES   (France)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Brain metabolism; Cerebral microdialysis; Hypertonic; Lactate; Traumatic brain injury

Indexed keywords

GLUCOSE; GLUTAMIC ACID; LACTATE SODIUM; LACTIC ACID; PYRUVIC ACID;

ADULT; ARTICLE; BRAIN INJURY; BRAIN METABOLISM; BRAIN TISSUE; CATHETER; CLINICAL ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENERGY METABOLISM; FEMALE; GLUCOSE BRAIN LEVEL; HEMODYNAMICS; HUMAN; INTRACRANIAL PRESSURE; MALE; MICRODIALYSIS; MIDDLE AGED; NEUROCHEMISTRY; NEUROPROTECTION; OXYGEN TENSION; PHASE 2 CLINICAL TRIAL; PROSPECTIVE STUDY; REGRESSION ANALYSIS; TRAUMATIC BRAIN INJURY; YOUNG ADULT; ARTIFICIAL VENTILATION; BRAIN; CLINICAL TRIAL; DIAGNOSTIC IMAGING; DRUG EFFECTS; FRONTAL LOBE; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; PROCEDURES; TIME FACTOR;

ADULT; BRAIN; BRAIN INJURIES, TRAUMATIC; ENERGY METABOLISM; FEMALE; FRONTAL LOBE; GLUCOSE; HUMANS; INFUSIONS, INTRAVENOUS; LACTIC ACID; MALE; MICRODIALYSIS; MIDDLE AGED; NEUROPROTECTION; PROSPECTIVE STUDIES; PYRUVIC ACID; RESPIRATION, ARTIFICIAL; SODIUM LACTATE; TIME FACTORS;

EID: 84899412718     PISSN: 03424642     EISSN: 14321238     Source Type: Journal    
DOI: 10.1007/s00134-013-3203-6     Document Type: Article

References (37)

1. Maas AI, Stocchetti N, Bullock R (2008) Moderate and severe traumatic brain injury in adults. Lancet Neurol 7:728-741
2. Bergsneider M, Hovda DA, Shalmon E, Kelly DF, Vespa PM, Martin NA, Phelps ME, McArthur DL, Caron MJ, Kraus JF, Becker DP (1997) Cerebral hyperglycolysis following severe traumatic brain injury in humans: a positron emission tomography study. J Neurosurg 86:241-251
3. Glenn TC, Kelly DF, Boscardin WJ, McArthur DL, Vespa P, Oertel M, Hovda DA, Bergsneider M, Hillered L, Martin NA (2003) Energy dysfunction as a predictor of outcome after moderate or severe head injury: indices of oxygen, glucose, and lactate metabolism. J Cereb Blood Flow Metab 23:1239-1250
4. Simpson IA, Carruthers A, Vannucci SJ (2007) Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 27:1766-1791
5. Oddo M, Schmidt JM, Carrera E, Badjatia N, Connolly ES, Presciutti M, Ostapkovich ND, Levine JM, Le Roux P, Mayer SA (2008) Impact of tight glycemic control on cerebral glucose metabolism after severe brain injury: a microdialysis study. Crit Care Med 36:3233-3238
6. Vespa PM, McArthur D, O'Phelan K, Glenn T, Etchepare M, Kelly D, Bergsneider M, Martin NA, Hovda DA (2003) Persistently low extracellular glucose correlates with poor outcome 6 months after human traumatic brain injury despite a lack of increased lactate: a microdialysis study. J Cereb Blood Flow Metab 23:865-877
7. Schurr A, West CA, Rigor BM (1988) Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240:1326-1328
8. Pellerin L, Pellegri G, Bittar PG, Charnay Y, Bouras C, Martin JL, Stella N, Magistretti PJ (1998) Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev Neurosci 20:291-299
9. Schurr A, Miller JJ, Payne RS, Rigor BM (1999) An increase in lactate output by brain tissue serves to meet the energy needs of glutamate-activated neurons. J Neurosci 19:34-39
10. Schurr A, Payne RS (2007) Lactate, not pyruvate, is neuronal aerobic glycolysis end product: an in vitro electrophysiological study. Neuroscience 147:613-619
11. Magistretti PJ (2008) Brain energy metabolism. In: Berg D, Bloom FE, du Lac S, Ghosh A, Spitzer NC, Squire LR (eds) Fundamental neurosciences. Academic, San Diego, pp 271-293
12. Gallagher CN, Carpenter KL, Grice P, Howe DJ, Mason A, Timofeev I, Menon DK, Kirkpatrick PJ, Pickard JD, Sutherland GR, Hutchinson PJ (2009) The human brain utilizes lactate via the tricarboxylic acid cycle: a 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain 132:2839-2849
13. Sala N, Suys T, Zerlauth JB, Bouzat P, Messerer M, Bloch J, Levivier M, Magistretti PJ, Meuli R, Oddo M (2013) Cerebral extracellular lactate increase is predominantly nonischemic in patients with severe traumatic brain injury. J Cereb Blood Flow Metab 33:1815-1822
14. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91:10625-10629
15. Pellerin L, Magistretti PJ (2012) Sweet sixteen for ANLS. J Cereb Blood Flow Metab 32:1152-1166
16. Chen T, Qian YZ, Rice A, Zhu JP, Di X, Bullock R (2000) Brain lactate uptake increases at the site of impact after traumatic brain injury. Brain Res 861:281-287
17. Jalloh I, Helmy A, Shannon RJ, Gallagher CN, Menon DK, Carpenter KL, Hutchinson PJ (2013) Lactate uptake by the injured human brain: evidence from an arteriovenous gradient and cerebral microdialysis study. J Neurotrauma. doi: 10.1089/neu.2013.2947
18. Bouzier-Sore AK, Voisin P, Canioni P, Magistretti PJ, Pellerin L (2003) Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J Cereb Blood Flow Metab 23:1298-1306
19. Rice AC, Zsoldos R, Chen T, Wilson MS, Alessandri B, Hamm RJ, Bullock MR (2002) Lactate administration attenuates cognitive deficits following traumatic brain injury. Brain Res 928:156-159
20. Bratton SL, Chestnut RM, Ghajar J, McConnell Hammond FF, Harris OA, Hartl R, Manley GT, Nemecek A, Newell DW, Rosenthal G, Schouten J, Shutter L, Timmons SD, Ullman JS, Videtta W, Wilberger JE, Wright DW (2007) Guidelines for the management of severe traumatic brain injury. IX. Cerebral perfusion thresholds. J Neurotrauma 24(Suppl 1):S59-S64
21. Bratton SL, Chestnut RM, Ghajar J, McConnell Hammond FF, Harris OA, Hartl R, Manley GT, Nemecek A, Newell DW, Rosenthal G, Schouten J, Shutter L, Timmons SD, Ullman JS, Videtta W, Wilberger JE, Wright DW (2007) Guidelines for the management of severe traumatic brain injury. VIII. Intracranial pressure thresholds. J Neurotrauma 24(Suppl 1):S55-S58
22. Boumezbeur F, Petersen KF, Cline GW, Mason GF, Behar KL, Shulman GI, Rothman DL (2010) The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J Neurosci 30:13983-13991
23. Smith D, Pernet A, Hallett WA, Bingham E, Marsden PK, Amiel SA (2003) Lactate: a preferred fuel for human brain metabolism in vivo. J Cereb Blood Flow Metab 23:658-664
24. Revelly JP, Tappy L, Martinez A, Bollmann M, Cayeux MC, Berger MM, Chiolero RL (2005) Lactate and glucose metabolism in severe sepsis and cardiogenic shock. Crit Care Med 33:2235-2240
25. Marshall LF, Marshall SB, Klauber MR, Van Berkum Clark M, Eisenberg H, Jane JA, Luerssen TG, Marmarou A, Foulkes MA (1992) The diagnosis of head injury requires a classification based on computed axial tomography. J Neurotrauma 9(Suppl 1):S287-S292
26. Oddo M, Levine JM, Frangos S, Maloney-Wilensky E, Carrera E, Daniel RT, Levivier M, Magistretti PJ, LeRoux PD (2012) Brain lactate metabolism in humans with subarachnoid hemorrhage. Stroke 43:1418-1421
27. Bergsneider M, Hovda DA, McArthur DL, Etchepare M, Huang SC, Sehati N, Satz P, Phelps ME, Becker DP (2001) Metabolic recovery following human traumatic brain injury based on FDG-PET: time course and relationship to neurological disability. J Head Trauma Rehabil 16:135-148
28. Rosenthal G, Hemphill JC 3rd, Sorani M, Martin C, Morabito D, Obrist WD, Manley GT (2008) Brain tissue oxygen tension is more indicative of oxygen diffusion than oxygen delivery and metabolism in patients with traumatic brain injury. Crit Care Med 36:1917-1924
29. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456:745-749
30. Hutchinson PJ, O'Connell MT, Seal A, Nortje J, Timofeev I, Al-Rawi PG, Coles JP, Fryer TD, Menon DK, Pickard JD, Carpenter KL (2009) A combined microdialysis and FDG-PET study of glucose metabolism in head injury. Acta Neurochir (Wien) 151:51-61; discussion 61
31. Vespa P, Bergsneider M, Hattori N, Wu HM, Huang SC, Martin NA, Glenn TC, McArthur DL, Hovda DA (2005) Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J Cereb Blood Flow Metab 25:763-774
32. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324:1029-1033
33. Dienel GA (2012) Brain lactate metabolism: the discoveries and the controversies. J Cereb Blood Flow Metab 32:1107-1138
34. McKenna MC (2007) The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain. J Neurosci Res 85:3347-3358
35. Roquilly A, Loutrel O, Cinotti R, Rosenczweig E, Flet L, Mahe PJ, Dumont R, Chupin AM, Peneaux C, Lejus C, Blanloeil Y, Volteau C, Asehnoune K (2013) Balanced versus chloride-rich solutions for fluid resuscitation in brain-injured patients: a randomized double-blind pilot study. Crit Care 17:R77
36. Ichai C, Armando G, Orban JC, Berthier F, Rami L, Samat-Long C, Grimaud D, Leverve X (2009) Sodium lactate versus mannitol in the treatment of intracranial hypertensive episodes in severe traumatic brain-injured patients. Intensive Care Med 35:471-479
37. Ichai C, Payen JF, Orban JC, Quintard H, Roth H, Legrand R, Francony G, Leverve XM (2013) Half-molar sodium lactate infusion to prevent intracranial hypertensive episodes in severe traumatic brain injured patients: a randomized controlled trial. Intensive Care Med 39:1413-1422