Glucose metabolism following human traumatic brain injury: methods of assessment and pathophysiological findings

Metabolic Brain Disease

Volumn 30, Issue 3, 2015, Pages 615-632

  Jalloh, Ibrahim ^a   Carpenter, Keri L H ^a   Helmy, Adel ^a   Carpenter, T Adrian ^a   Menon, David K ^a   Hutchinson, Peter J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

13C labelling; Glucose; Magnetic resonance spectroscopy; Microdialysis; Positron emission tomography; Traumatic brain injury

Indexed keywords

GLUCOSE;

ANIMAL; AUTORADIOGRAPHY; BRAIN INJURIES; ENERGY METABOLISM; EXTRACELLULAR FLUID; HUMAN; METABOLISM; MICRODIALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; PROCEDURES;

ANIMALS; AUTORADIOGRAPHY; BRAIN INJURIES; ENERGY METABOLISM; EXTRACELLULAR FLUID; GLUCOSE; HUMANS; MAGNETIC RESONANCE IMAGING; MICRODIALYSIS; POSITRON-EMISSION TOMOGRAPHY;

EID: 84939949698     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-014-9628-y     Document Type: Review

References (96)

1. Aaen GS, Holshouser BA, Sheridan C et al (2010) Magnetic resonance spectroscopy predicts outcomes for children with nonaccidental trauma. Pediatrics 125:295–303. doi:10.1542/peds. 2008-3312
2. Alessandri B, Rice AC, Levasseur J et al (2002) Cyclosporin A improves brain tissue oxygen consumption and learning/memory performance after lateral fluid percussion injury in rats. J Neurotrauma 19:829–841. doi:10.1089/08977150260190429
3. Andersen BJ, Marmarou A (1992) Post-traumatic selective stimulation of glycolysis. Brain Res 585:184–189
4. Ashwal S, Holshouser BA, Shu SK et al (2000) Predictive value of proton magnetic resonance spectroscopy in pediatric closed head injury. Pediatr Neurol 23:114–125
5. Bartnik BL, Lee SM, Hovda DA, Sutton RL (2007) The fate of glucose during the period of decreased metabolism after fluid percussion injury: a 13C NMR study. J Neurotrauma 24:1079–1092. doi:10.1089/neu.2006.0210
6. Bartnik BL, Sutton RL, Fukushima M et al (2005) Upregulation of pentose phosphate pathway and preservation of tricarboxylic acid cycle flux after experimental brain injury. J Neurotrauma 22:1052–1065. doi:10.1089/neu.2005.22.1052
7. Bergsneider M, Hovda DA, Lee SM et al (2000) Dissociation of cerebral glucose metabolism and level of consciousness during the period of metabolic depression following human traumatic brain injury. J Neurotrauma 17:389–401. doi:10.1089/neu.2000.17.389
8. Bergsneider M, Hovda DA, Shalmon E et al (1997) Cerebral hyperglycolysis following severe traumatic brain injury in humans: a positron emission tomography study. J Neurosurg 86:241–251. doi:10.3171/jns.1997.86.2.0241
9. Bouzat P, Sala N, Suys T et al (2014) Cerebral metabolic effects of exogenous lactate supplementation on the injured human brain. Intensive Care Med 40:412–421. doi:10.1007/s00134-013-3203-6
10. Cadoux-Hudson TA, Wade D, Taylor DJ et al (1990) Persistent metabolic sequelae of severe head injury in humans in vivo. Acta Neurochir (Wien) 104:1–7
11. Carpenter KLH, Jalloh I, Gallagher CN et al (2014) (13)C-labelled microdialysis studies of cerebral metabolism in TBI patients. Eur J Pharm Sci 57:87–97. doi:10.1016/j.ejps.2013.12.012
12. Cecil KM, Hills EC, Sandel ME et al (1998) Proton magnetic resonance spectroscopy for detection of axonal injury in the splenium of the corpus callosum of brain-injured patients. J Neurosurg 88:795–801. doi:10.3171/jns.1998.88.5.0795
13. Chen T, Qian YZ, Di X et al (2000) Evidence for lactate uptake after rat fluid percussion brain injury. Acta Neurochir Suppl 76:359–364
14. Chesnut RM, Marshall LF, Klauber MR et al (1993) The role of secondary brain injury in determining outcome from severe head injury. J Trauma Inj Infect Crit Care 34:216–222
15. Coles JP, Fryer TD, Smielewski P et al (2004) Incidence and mechanisms of cerebral ischemia in early clinical head injury. J Cereb Blood Flow Metab 24:202–211. doi:10.1097/01.WCB.0000103022.98348.24
16. Cruz J (1995) An additional therapeutic effect of adequate hyperventilation in severe acute brain trauma: normalization of cerebral glucose uptake. J Neurosurg 82:379–385. doi:10.3171/jns.1995.82.3.0379
17. Diaz-Parejo P, Ståhl N, Xu W, et al. (2003) Cerebral energy metabolism during transient hyperglycemia in patients with severe brain trauma. Intensive Care Med 29:544–550. doi:10.1007/s00134-003-1669-3
18. Dusick JR, Glenn TC, Lee WNP et al (2007) Increased pentose phosphate pathway flux after clinical traumatic brain injury: a [1,2-13C2]glucose labeling study in humans. J Cereb Blood Flow Metab 27:1593–1602. doi:10.1038/sj.jcbfm.9600458
19. Eleff S, Kennaway NG, Buist NR et al (1984) 31P NMR study of improvement in oxidative phosphorylation by vitamins K3 and C in a patient with a defect in electron transport at complex III in skeletal muscle. Proc Natl Acad Sci U S A 81:3529–3533
20. Ferris EB, Engel GL (1946) The validity of internal jugular venous blood in studies of cerebral metabolism and blood flow in man. Am J Physiol 147:517–521
21. Gallagher CN, Carpenter KLH, Grice P et al (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. doi:10.1093/brain/awp202
22. Garnett MR, Blamire AM, Corkill RG et al (2000) Early proton magnetic resonance spectroscopy in normal-appearing brain correlates with outcome in patients following traumatic brain injury. Brain 123:2046–2054. doi:10.1093/brain/123.10.2046
23. Garnett MR, Corkill RG, Blamire AM et al (2001) Altered cellular metabolism following traumatic brain injury: a magnetic resonance spectroscopy study. J Neurotrauma 18:231–240. doi:10.1089/08977150151070838
24. Glenn TC, Kelly DF, Boscardin WJ, et al (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 1239–1250. doi:10.1097/01.WCB.0000089833.23606.7F
25. Gruetter R, Novotny EJ, Boulware SD et al (2002) Localized 13C NMR spectroscopy in the human brain of amino acid labeling from d-[1-13C]Glucose. J Neurochem 63:1377–1385. doi:10.1046/j.1471-4159.1994.63041377.x
26. Hall ED, Andrus PK, Yonkers PA (1993) Brain hydroxyl radical generation in acute experimental head injury. J Neurochem 60:588–594. doi:10.1111/j.1471-4159.1993.tb03189.x
27. Hamilton G, Allsop JM, Patel N, et al. (2006) Variations due to analysis technique in intracellular pH measurements in simulated and in vivo 31P MR spectra of the human brain. J Magn Reson Imaging 23:459–464. doi:10.1002/jmri.20524
28. Hattori N, Huang S-C, Wu H-M et al (2003) Correlation of regional metabolic rates of glucose with glasgow coma scale after traumatic brain injury. J Nucl Med 44:1709–1716
29. Heath DL, Vink R (1995) Impact acceleration-induced severe diffuse axonal injury in rats: characterization of phosphate metabolism and neurologic outcome. J Neurotrauma 12:1027–1034
30. Herrero-Mendez A, Almeida A, Fernández E et al (2009) The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C–Cdh1. Nat Cell Biol 11:747–752. doi:10.1038/ncb1881
31. Hetherington HP, Spencer DD, Vaughan JT, Pan JW (2001) Quantitative31P spectroscopic imaging of human brain at 4 Tesla: assessment of gray and white matter differences of phosphocreatine and ATP. Magn Reson Med 45:46–52. doi:10.1002/1522-2594(200101)45:1<46::AID-MRM1008>3.0.CO;2-N
32. Hlatky R, Valadka AB, Goodman JC et al (2004) Patterns of energy substrates during ischemia measured in the brain by microdialysis. J Neurotrauma 21:894–906. doi:10.1089/0897715041526195
33. Holbein M, Béchir M, Ludwig S et al (2009) Differential influence of arterial blood glucose on cerebral metabolism following severe traumatic brain injury. Crit Care 13:R13. doi:10.1186/cc7711
34. Huang SC, Phelps ME, Hoffman EJ et al (1980) Noninvasive determination of local cerebral metabolic rate of glucose in man. Am J Physiol 238:E69–E82
35. Hutchinson PJ, Gupta AK, Fryer TF et al (2002) Correlation between cerebral blood flow, substrate delivery, and metabolism in head injury: a combined microdialysis and triple oxygen positron emission tomography study. J Cereb Blood Flow Metab 22:735–745. doi:10.1097/00004647-200206000-00012
36. Hutchinson PJ, O’Connell MT, Seal A et al (2009) A combined microdialysis and FDG-PET study of glucose metabolism in head injury. Acta Neurochir (Wien) 151:51–61. doi:10.1007/s00701-008-0169-1, discussion 61
37. Jalloh I, Helmy A, Shannon RJ et al (2013) Lactate uptake by the injured human brain—evidence from an arterio-venous gradient and cerebral microdialysis study. J Neurotrauma 30:2031–2037. doi:10.1089/neu.2013.2947
38. Kaibara T, Sutherland GR, Colbourne F, Tyson RL (1999) Hypothermia: depression of tricarboxylic acid cycle flux and evidence for pentose phosphate shunt upregulation. J Neurosurg 90:339–347. doi:10.3171/jns.1999.90.2.0339
39. Katayama Y, Becker DP, Tamura T, Hovda DA (1990) Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73:889–900. doi:10.3171/jns.1990.73.6.0889
40. Kato T, Nakayama N, Yasokawa Y et al (2007) Statistical image analysis of cerebral glucose metabolism in patients with cognitive impairment following diffuse traumatic brain injury. J Neurotrauma 24:919–926. doi:10.1089/neu.2006.0203
41. Kawamata T, Katayama Y, Hovda DA et al (1992) Administration of excitatory amino acid antagonists via microdialysis attenuates the increase in glucose utilization seen following concussive brain injury. J Cereb Blood Flow Metab 12:12–24. doi:10.1038/jcbfm.1992.3
42. Kety SS, Schmidt CF (1948) The nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure and normal values. J Clin Invest 27:476–483. doi:10.1172/JCI101994
43. Kolias AG, Guilfoyle MR, Helmy A et al (2013) Traumatic brain injury in adults. Pract Neurol 13:228–235. doi:10.1136/practneurol-2012-000268
44. Lammertsma AA, Brooks DJ, Frackowiak RSJ et al (1987) Measurement of glucose utilisation with [18F]2-Fluoro-2-Deoxy-D-Glucose: a comparison of different. Anal Methods 7:161–172. doi:10.1038/jcbfm.1987.39
45. Larsen TS, Rasmussen P, Overgaard M et al (2008) Non-selective β-adrenergic blockade prevents reduction of the cerebral metabolic ratio during exhaustive exercise in humans. J Physiol 586:2807–2815. doi:10.1113/jphysiol.2008.151449
46. Leegsma-Vogt G, Venema K, Postema F, Korf J (2001) Monitoring arterio-venous differences of glucose and lactate in the anesthetized rat with or without brain damage with ultrafiltration and biosensor technology. J Neurosci Res 66:795–802. doi:10.1002/jnr.10046
47. Lewén A, Fujimura M, Sugawara T et al (2001) Oxidative stress-dependent release of mitochondrial cytochrome c after traumatic brain injury. Journal of Cerebral Blood Flow and Metabolism 21:914–920. doi:10.1097/00004647-200108000-00003
48. Maas AI, Maas A, Stocchetti N et al (2008) Moderate and severe traumatic brain injury in adults. Lancet Neurol. doi:10.1016/S1474-4422(08)70164-9
49. Marino S, Ciurleo R, Bramanti P et al (2010) 1H-MR spectroscopy in traumatic brain injury. Neurocrit Care 14:127–133. doi:10.1007/s12028-010-9406-6
50. Marino S, Zei E, Battaglini M et al (2007) Acute metabolic brain changes following traumatic brain injury and their relevance to clinical severity and outcome. JNNP 78:501–507. doi:10.1136/jnnp.2006.099796
51. Marklund N, Clausen F, Lewander T, Hillered L (2001) Monitoring of reactive oxygen species production after traumatic brain injury in rats with microdialysis and the 4-hydroxybenzoic acid trapping method. J Neurotrauma 18:1217–1227. doi:10.1089/089771501317095250
52. Marklund N, Sihver S, Hovda DA et al (2009) Increased cerebral uptake of [18F]Fluoro-Deoxyglucose but not [1–14C]Glucose early following traumatic brain injury in rats. J Neurotrauma 26:1281–1293. doi:10.1089/neu.2008.0827
53. Marmarou A, Anderson RL, Ward JD et al (2009) Impact of ICP instability and hypotension on outcome in patients with severe head trauma. J Neurosurg 75:s59–s66. doi:10.3171/sup.1991.75.1s.0s59
54. Mason GF, Gruetter R, Rothman DL et al (1995) Simultaneous determination of the rates of the TCA cycle, glucose utilization, |[alpha]|-ketoglutarate|[sol]|glutamate exchange, and glutamine synthesis in human brain by NMR. J Cereb Blood Flow Metab 15:12–25. doi:10.1038/jcbfm.1995.2
55. Meierhans R, Béchir M, Ludwig S et al (2010) Brain metabolism is significantly impaired at blood glucose below 6 mM and brain glucose below 1 mM in patients with severe traumatic brain injury. Crit Care 14:R13. doi:10.1186/cc8869
56. Meierhans R, Brandi G, Fasshauer M et al (2012) Arterial lactate above 2 mM is associated with increased brain lactate and decreased brain glucose in patients with severe traumatic brain injury. Minerva Anestesiol 78:185–193
57. Moreno A, Blüml S, Hwang JH, Ross BD (2001) Alternative 1‐13C glucose infusion protocols for clinical 13C MRS examinations of the brain. Magn Reson Med 46:39–48. doi:10.1002/mrm.1158
58. Newcombe VFJ, Williams GB, Outtrim JG et al (2013) Microstructural basis of contusion expansion in traumatic brain injury: insights from diffusion tensor imaging. J Cereb Blood Flow Metab 33:855–862. doi:10.1038/jcbfm.2013.11
59. Nortje J, Coles JP, Timofeev I et al (2008) Effect of hyperoxia on regional oxygenation and metabolism after severe traumatic brain injury: preliminary findings*. Crit Care Med 36:273–281. doi:10.1097/01.CCM.0000292014.60835.15
60. Osteen CL, Moore AH, Prins ML, Hovda DA (2004) Age-dependency of 45Calcium accumulation following lateral fluid percussion: acute and delayed patterns. http://dxdoiorg/10.1089/08977150150502587
61. Pandya JD, Readnower RD, Patel SP et al (2014) N-acetylcysteine amide confers neuroprotection, improves bioenergetics and behavioral outcome following TBI. Exp Neurol 257:106–113. doi:10.1016/j.expneurol.2014.04.020
62. Paraforou T, Paterakis K, Fountas K et al (2011) Cerebral perfusion pressure, microdialysis biochemistry and clinical outcome in patients with traumatic brain injury. BMC Res Notes 4:540. doi:10.1186/1756-0500-4-540
63. Patlak CS, Blasberg RG (1985) Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J Cereb Blood Flow Metab 5:584–590. doi:10.1038/jcbfm.1985.87
64. Pattinson K, Wynne-Jones G, Imray C (2005) Monitoring intracranial pressure, perfusion and metabolism. Contin Educ Anaesth Crit Care Pain 5:130–133. doi:10.1093/bjaceaccp/mki037
65. 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
66. Phelps ME (1991) PET: a biological imaging technique. Neurochem Res 16:929–940
67. Prins ML, Giza CC (2006) Induction of monocarboxylate transporter 2 expression and ketone transport following traumatic brain injury in juvenile and adult rats. Dev Neurosci 28:447–456. doi:10.1159/000094170
68. Roozenbeek B, Maas AIR, Menon DK (2013) Changing patterns in the epidemiology of traumatic brain injury. Nat Publ Group 9:231–236. doi:10.1038/nrneurol.2013.22
69. Rostami E, Bellander B-M (2011) Monitoring of glucose in brain, adipose tissue, and peripheral blood in patients with traumatic brain injury: a microdialysis study. J Diabetes Sci Technol 5:596–604
70. Rothman DL, De Feyter HM, de Graaf RA et al (2011) 13C MRS studies of neuroenergetics and neurotransmitter cycling in humans. NMR Biomed 24:943–957. doi:10.1002/nbm.1772
71. Sampol D, Ostrofet E, Jobin M-L et al (2013) Glucose and lactate metabolism in the awake and stimulated rat: a (13)C-NMR study. Front Neuroenerg 5:5. doi:10.3389/fnene.2013.00005
72. Satchell MA, Zhang X, Kochanek PM et al (2003) A dual role for poly‐ADP‐ribosylation in spatial memory acquisition after traumatic brain injury in mice involving NAD+ depletion and ribosylation of 14‐3‐3γ. J Neurochem 85:697–708. doi:10.1046/j.1471-4159.2003.01707.x
73. Scheff SW, Sullivan PG (1999) Cyclosporin A significantly ameliorates cortical damage following experimental traumatic brain injury in rodents. J Neurotrauma. doi:10.1089/neu.1999.16.783
74. Schönfeld P, Reiser G (2013) Why does brain metabolism not favor burning of fatty acids to provide energy? Reflections on disadvantages of the use of free fatty acids as fuel for brain. J Cereb Blood Flow Metab 33:1493–1499. doi:10.1038/jcbfm.2013.128
75. Sokoloff L, Reivich M, Kennedy C et al (1977) The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem 28:897–916. doi:10.1111/j.1471-4159.1977.tb10649.x
76. Stein NR, McArthur DL, Etchepare M, Vespa PM (2012) Early cerebral metabolic crisis after TBI influences outcome despite adequate hemodynamic resuscitation. Neurocrit Care 17:49–57. doi:10.1007/s12028-012-9708-y
77. Stocchetti N, Furlan A, Volta F (1996) Hypoxemia and arterial hypotension at the accident scene in head injury. J Trauma Inj Infect Crit Care 40:764–767
78. Sullivan PG, KELLER JN, MATTSON MP, Scheff SW (1998) Traumatic brain injury alters synaptic homeostasis: implications for impaired mitochondrial and transport function. J Neurotrauma 15:789–798. doi:10.1089/neu.1998.15.789
79. Sunami K, Nakamura T, Ozawa Y et al (1989) Hypermetabolic state following experimental head injury. Neurosurg Rev 12(Suppl 1):400–411. doi:10.1007/BF01790682
80. Tagliaferri F, Compagnone C, Korsic M et al (2006) A systematic review of brain injury epidemiology in Europe. Acta Neurochir (Wien) 148:255–268. doi:10.1007/s00701-005-0651-y, discussion 268
81. Timofeev I, Carpenter KLH, Nortje J et al (2011a) Cerebral extracellular chemistry and outcome following traumatic brain injury: a microdialysis study of 223 patients. Brain 134:484–494. doi:10.1093/brain/awq353
82. Timofeev I, Czosnyka M, Carpenter KLH et al (2011b) Interaction between brain chemistry and physiology after traumatic brain injury: impact of autoregulation and microdialysis catheter location. J Neurotrauma 28:849–860. doi:10.1089/neu.2010.1656
83. Tyson RL, Gallagher CN, Sutherland GR (2003) 13C-Labeled substrates and the cerebral metabolic compartmentalization of acetate and lactate. Brain Res 992:43–52. doi:10.1016/j.brainres.2003.08.027
84. Unterberg AW, Stover J, Kress B, Kiening KL (2004) Edema and brain trauma. Neuroscience 129:1021–1029. doi:10.1016/j.neuroscience.2004.06.046
85. Vespa P, Bergsneider M, Hattori N et al (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. doi:10.1038/sj.jcbfm.9600073
86. Vespa P, Boonyaputthikul R, McArthur DL et al (2006) Intensive insulin therapy reduces microdialysis glucose values without altering glucose utilization or improving the lactate/pyruvate ratio after traumatic brain injury*. Crit Care Med 34:850–856. doi:10.1097/01.CCM.0000201875.12245.6F
87. Vespa PM, McArthur D, O'Phelan K, et al (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 865–877. doi:10.1097/01.WCB.0000076701.45782.EF
88. Vespa P, McArthur D, Stein N, et al. (2012) Tight glycemic control increases metabolic distress in traumatic brain injury: a randomized controlled within-subjects trial. Crit Care Med 40:1923–1929. doi:10.1097/CCM.0b013e31824e0fcc
89. Vink R, McIntosh TK, Weiner MW, Faden AI (1987) Effects of traumatic brain injury on cerebral high-energy phosphates and pH: A 31P magnetic resonance spectroscopy study. J Cereb Blood Flow Metab 7:563–571. doi:10.1038/jcbfm.1987.106
90. Wu H-M, Huang S-C, Hattori N et al (2004) Selective metabolic reduction in gray matter acutely following human traumatic brain injury. J Neurotrauma 21:149–161. doi:10.1089/089771504322778613
91. Wu H-M, Huang S-C, Vespa P et al (2013) Redefining the pericontusional penumbra following traumatic brain injury: evidence of deteriorating metabolic derangements based on positron emission tomography. J Neurotrauma 30:352–360. doi:10.1089/neu.2012.2610
92. Xiong Y, Gu Q, Peterson PL et al (1997) Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J Neurotrauma 14:23–34. doi:10.1089/neu.1997.14.23
93. Xiong Y, Mahmood A, Chopp M (2013) Animal models of traumatic brain injury. Nat Rev Neurosci 14:128–142. doi:10.1038/nrn3407
94. Yokobori S, Watanabe A, Matsumoto G et al (2011) Time course of recovery from cerebral vulnerability after severe traumatic brain injury: a microdialysis study. J Trauma Inj Infect Crit Care 71:1235–1240. doi:10.1097/TA.0b013e3182140dd7
95. Zauner A, Doppenberg EM, Woodward JJ et al (1997) Continuous monitoring of cerebral substrate delivery and clearance: initial experience in 24 patients with severe acute brain injuries. Neurosurgery 41:1082–1091, discussion 1091–3
96. Zhang J, Mitsis EM, Chu K et al (2010) Statistical parametric mapping and cluster counting analysis of [18F] FDG-PET imaging in traumatic brain injury. J Neurotrauma 27:35–49. doi:10.1089/neu.2009.1049