Cerebral hyperglycolysis following severe traumatic brain injury in humans: a positron emission tomography study

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✓ Experimental traumatic brain injury studies have shown that cerebral hyperglycolysis is a pathophysiological response to injury-induced ionic and neurochemical cascades. This finding has important implications regarding cellular viability, vulnerability to secondary insults, and the functional capability of affected regions. Prior to this study, posttraumatic hyperglycolysis had not been detected in humans.

The characteristics and incidence of cerebral hyperglycolysis were determined in 28 severely head injured patients using [18F]fluorodeoxyglucose—positron emission tomography (FDG-PET). The local cerebral metabolic rate of glucose (CMRG) was calculated using a standard compartmental model. In six of the 28 patients, the global cerebral metabolic rate of oxygen (CMRO2) was determined by the simultaneous measurements of arteriovenous differences of oxygen and cerebral blood flow (xenon-133). Hyperglycolysis, defined as an increase in glucose utilization that measures two standard deviations above expected levels, was documented in all six patients in whom both FDG-PET and CMRO2 determinations were made within 8 days of injury. Five additional patients were found to have localized areas of hyperglycolysis adjacent to focal mass lesions. Within the 1st week following the injury, 56% of patients studied had presumptive evidence of hyperglycolysis.

The results of this study indicate that the metabolic state of the traumatically injured brain should be defined differentially in terms of glucose and oxygen metabolism. The use of FDG-PET demonstrates that hyperglycolysis occurs both regionally and globally following severe head injury in humans. The results of this clinical study directly complement those previously reported in experimental brain-injury studies, indicating the capability of imaging a fundamental component of cellular pathophysiology characteristic of head injury.

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Contributor Notes

Address reprint requests to: Marvin Bergsneider, M.D., Division of Neurosurgery, University of California at Los Angeles, 18–218 NPI, Los Angeles, California 90095.
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References
  • 1.

    Ackermann RFLear JL: Glycolysis-induced discordance between glucose metabolic rates measured with radiolabelled fluorodeoxyglucose and glucose. J Cereb Blood Flow Metab 9:7747851989Ackermann RF Lear JL: Glycolysis-induced discordance between glucose metabolic rates measured with radiolabelled fluorodeoxyglucose and glucose. J Cereb Blood Flow Metab 9:774–785 1989

    • Search Google Scholar
    • Export Citation
  • 2.

    Alavi ALangfitt TFazekas Fet al: Correlative studies of head trauma (HT) with PET, MRI, and XCT. J Nucl Med 27:9199201986 (Abstract)Alavi A Langfitt T Fazekas F et al: Correlative studies of head trauma (HT) with PET MRI and XCT. J Nucl Med 27:919–920 1986 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 3.

    Andersen BJMarmarou A: Isolated stimulation of glycolysis following traumatic brain injury in Hoff JTBetz AL (eds): Intracranial Pressure VII. Berlin: Springer-Verlag1989 pp 575580Andersen BJ Marmarou A: Isolated stimulation of glycolysis following traumatic brain injury in Hoff JT Betz AL (eds): Intracranial Pressure VII. Berlin: Springer-Verlag 1989 pp 575–580

    • Search Google Scholar
    • Export Citation
  • 4.

    Andersen BJMarmarou A: Post-traumatic selective stimulation of glycolysis. Brain Res 585:1841891992Andersen BJ Marmarou A: Post-traumatic selective stimulation of glycolysis. Brain Res 585:184–189 1992

    • Search Google Scholar
    • Export Citation
  • 5.

    Ashford CADixon KC: The effect of potassium on the glucolysis of brain tissue with reference to the Pasteur effect. Biochem J 29:1571681935Ashford CA Dixon KC: The effect of potassium on the glucolysis of brain tissue with reference to the Pasteur effect. Biochem J 29:157–168 1935

    • Search Google Scholar
    • Export Citation
  • 6.

    Association for the Advancement of Automotive Medicine: The Abbreviated Injury Scale 1990 Revision. Des Plaines, Ill: Association for the Advancement of Automotive Medicine1990Association for the Advancement of Automotive Medicine: The Abbreviated Injury Scale 1990 Revision. Des Plaines Ill: Association for the Advancement of Automotive Medicine 1990

    • Search Google Scholar
    • Export Citation
  • 7.

    Ben Yoseph OBoxer PARoss BD: Assessment of the role of the glutathione and pentose phosphate pathways in the protection of primary cerebrocortical cultures from oxidative stress. J Neurochem 66:232923371996Ben Yoseph O Boxer PA Ross BD: Assessment of the role of the glutathione and pentose phosphate pathways in the protection of primary cerebrocortical cultures from oxidative stress. J Neurochem 66:2329–2337 1996

    • Search Google Scholar
    • Export Citation
  • 8.

    Ben Yoseph OCamp DMRobinson TEet al: Dynamic measurements of cerebral pentose phosphate pathway activity in vivo using [1,6-13C2,6,6-2H2]glucose and microdialysis. J Neurochem 64:133613421995Ben Yoseph O Camp DM Robinson TE et al: Dynamic measurements of cerebral pentose phosphate pathway activity in vivo using [16-13C266-2H2]glucose and microdialysis. J Neurochem 64:1336–1342 1995

    • Search Google Scholar
    • Export Citation
  • 9.

    Betz ALGilboe DDDrewes LR: Kinetics of anoxia on net uptake and unidirectional transport of glucose into the isolated dog brain. Brain Res 67:3073161974Betz AL Gilboe DD Drewes LR: Kinetics of anoxia on net uptake and unidirectional transport of glucose into the isolated dog brain. Brain Res 67:307–316 1974

    • Search Google Scholar
    • Export Citation
  • 10.

    Bouma GJMuizelaar JPChoi SCet al: Cerebral circulation and metabolism after severe traumatic brain injury: the elusive role of ischemia. J Neurosurg 75:6856931991Bouma GJ Muizelaar JP Choi SC et al: Cerebral circulation and metabolism after severe traumatic brain injury: the elusive role of ischemia. J Neurosurg 75:685–693 1991

    • Search Google Scholar
    • Export Citation
  • 11.

    Brodersen PJørgensen EO: Cerebral blood flow and oxygen uptake, and cerebrospinal fluid biochemistry in severe coma. J Neurol Neurosurg Psychiatry 37:3843911974Brodersen P Jørgensen EO: Cerebral blood flow and oxygen uptake and cerebrospinal fluid biochemistry in severe coma. J Neurol Neurosurg Psychiatry 37:384–391 1974

    • Search Google Scholar
    • Export Citation
  • 12.

    Bullock RStatham PPatterson Jet al: The time course of vasogenic oedema after focal human head injury—evidence from SPECT mapping of blood brain barrier defects. Acta Neurochir Suppl 51:2862881990Bullock R Statham P Patterson J et al: The time course of vasogenic oedema after focal human head injury—evidence from SPECT mapping of blood brain barrier defects. Acta Neurochir Suppl 51:286–288 1990

    • Search Google Scholar
    • Export Citation
  • 13.

    Bullock RZanner ATsnji Oet al: Patterns of excitatory amino acid release and ionic flux after severe human head injury in Tsubokawa TMarmarou ARobertson Cet al (eds): Neurochemical Monitoring in the Intensive Care Unit. Tokyo: Springer-Verlag1995 pp 6471Bullock R Zanner A Tsnji O et al: Patterns of excitatory amino acid release and ionic flux after severe human head injury in Tsubokawa T Marmarou A Robertson C et al (eds): Neurochemical Monitoring in the Intensive Care Unit. Tokyo: Springer-Verlag 1995 pp 64–71

    • Search Google Scholar
    • Export Citation
  • 14.

    Chugani HTShewmon DAKhanna Set al: Interictal and postictal focal hypermetabolism on positron emission tomography. Pediatr Neurol 9:10151993Chugani HT Shewmon DA Khanna S et al: Interictal and postictal focal hypermetabolism on positron emission tomography. Pediatr Neurol 9:10–15 1993

    • Search Google Scholar
    • Export Citation
  • 15.

    Cortez SCMcIntosh TKNoble LJ: Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res 482:2712821989Cortez SC McIntosh TK Noble LJ: Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res 482:271–282 1989

    • Search Google Scholar
    • Export Citation
  • 16.

    Cox SBWoolsey TARovainen CM: Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J Cereb Blood Flow Metab 13:8999131993Cox SB Woolsey TA Rovainen CM: Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J Cereb Blood Flow Metab 13:899–913 1993

    • Search Google Scholar
    • Export Citation
  • 17.

    DeSalles AAFMuizelaar JPYoung HF: Hyperglycemia, cerebrospinal fluid lactic acidosis, and cerebral blood flow in severely head-injured patients. Neurosurgery 21:45501987DeSalles AAF Muizelaar JP Young HF: Hyperglycemia cerebrospinal fluid lactic acidosis and cerebral blood flow in severely head-injured patients. Neurosurgery 21:45–50 1987

    • Search Google Scholar
    • Export Citation
  • 18.

    Engel J JrKuhl DEPhelps MEet al: Local cerebral metabolism during partial seizures. Neurology 33:4004131983Engel J Jr Kuhl DE Phelps ME et al: Local cerebral metabolism during partial seizures. Neurology 33:400–413 1983

    • Search Google Scholar
    • Export Citation
  • 19.

    Evans MCMeldrum BS: Regional brain glucose metabolism in chemically-induced seizures in the rat. Brain Res 297:2352451984Evans MC Meldrum BS: Regional brain glucose metabolism in chemically-induced seizures in the rat. Brain Res 297:235–245 1984

    • Search Google Scholar
    • Export Citation
  • 20.

    Ginsberg MDReivich M: Use of the 2-deoxyglucose method of local cerebral glucose utilization in the abnormal brain: evaluation of the lumped constant during ischemia. Acta Neurol Scand 70:2262271979 (Abstract)Ginsberg MD Reivich M: Use of the 2-deoxyglucose method of local cerebral glucose utilization in the abnormal brain: evaluation of the lumped constant during ischemia. Acta Neurol Scand 70:226–227 1979 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 21.

    Gonzalez MFSharp FR: Vibrissae tactile stimulation: (14C) 2-deoxyglucose uptake in rat brainstem, thalamus, and cortex. J Comp Neurol 231:4574721985Gonzalez MF Sharp FR: Vibrissae tactile stimulation: (14C) 2-deoxyglucose uptake in rat brainstem thalamus and cortex. J Comp Neurol 231:457–472 1985

    • Search Google Scholar
    • Export Citation
  • 22.

    Goodman JRobertson DGopinath Set al: Measurement of lactic acid and amino acids in the cerebral cortex of head injured patients using microdialysis in Tsubokawa TMarmarou ARobertson Cet al (eds): Neurochemical Monitoring in the Intensive Care Unit. Tokyo: Springer-Verlag1995 pp 7886Goodman J Robertson D Gopinath S et al: Measurement of lactic acid and amino acids in the cerebral cortex of head injured patients using microdialysis in Tsubokawa T Marmarou A Robertson C et al (eds): Neurochemical Monitoring in the Intensive Care Unit. Tokyo: Springer-Verlag 1995 pp 78–86

    • Search Google Scholar
    • Export Citation
  • 23.

    Hall EDAndrus PKYonkers PA: Brain hydroxyl radical generation in acute experimental head injury. J Neurochem 60:5885941993Hall ED Andrus PK Yonkers PA: Brain hydroxyl radical generation in acute experimental head injury. J Neurochem 60:588–594 1993

    • Search Google Scholar
    • Export Citation
  • 24.

    Hovda DA: Metabolic dysfunction in Narayan RKWilberger JE JrPovlishock JT (eds): Neurotrauma. New York: McGraw-Hill1996 pp 14591478Hovda DA: Metabolic dysfunction in Narayan RK Wilberger JE Jr Povlishock JT (eds): Neurotrauma. New York: McGraw-Hill 1996 pp 1459–1478

    • Search Google Scholar
    • Export Citation
  • 25.

    Hovda DABecker DPKatayama Y: Secondary injury and acidosis. J Neurotrauma 9 (Suppl 1):S47S601992Hovda DA Becker DP Katayama Y: Secondary injury and acidosis. J Neurotrauma 9 (Suppl 1):S47–S60 1992

    • Search Google Scholar
    • Export Citation
  • 26.

    Hovda DAKatayama YYoshino Aet al: Pre- or postsynaptic blocking of glutamatergic functioning prevents the increase in glucose utilization following concussive brain injury in Globus MDietrich WD (ed): The Role of Neurotransmitters in Brain Injury. New York: Plenum Press1993 pp 327332Hovda DA Katayama Y Yoshino A et al: Pre- or postsynaptic blocking of glutamatergic functioning prevents the increase in glucose utilization following concussive brain injury in Globus M Dietrich WD (ed): The Role of Neurotransmitters in Brain Injury. New York: Plenum Press 1993 pp 327–332

    • Search Google Scholar
    • Export Citation
  • 27.

    Huang SCPhelps MEHoffman EJet al: Error sensitivity of fluorodeoxyglucose method for measurement of cerebral metabolic rate of glucose. J Cereb Blood Flow Metab 1:3914011981Huang SC Phelps ME Hoffman EJ et al: Error sensitivity of fluorodeoxyglucose method for measurement of cerebral metabolic rate of glucose. J Cereb Blood Flow Metab 1:391–401 1981

    • Search Google Scholar
    • Export Citation
  • 28.

    Huang SCPhelps MEHoffman EJet al: Noninvasive determination of local cerebral metabolic rate of glucose in man. Am J Physiol 238:E69E821980Huang SC Phelps ME Hoffman EJ et al: Noninvasive determination of local cerebral metabolic rate of glucose in man. Am J Physiol 238:E69–E82 1980

    • Search Google Scholar
    • Export Citation
  • 29.

    Inao SMarmarou AClarke GDet al: Production and clearance of lactate from brain tissue, cerebrospinal fluid, and serum following experimental brain injury. J Neurosurg 69:7367441988Inao S Marmarou A Clarke GD et al: Production and clearance of lactate from brain tissue cerebrospinal fluid and serum following experimental brain injury. J Neurosurg 69:736–744 1988

    • Search Google Scholar
    • Export Citation
  • 30.

    Inglis FKuroda YBullock R: Glucose hypermetabolism after acute subdural hematoma is ameliorated by a competitive NMDA antagonist. J Neurotrauma 9:75841992Inglis F Kuroda Y Bullock R: Glucose hypermetabolism after acute subdural hematoma is ameliorated by a competitive NMDA antagonist. J Neurotrauma 9:75–84 1992

    • Search Google Scholar
    • Export Citation
  • 31.

    Katayama YBecker DPTamura Tet al: Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73:8899001990Katayama Y Becker DP Tamura T et al: Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73:889–900 1990

    • Search Google Scholar
    • Export Citation
  • 32.

    Katayama YCheung MKAlves Aet al: Ion fluxes and cell swelling in experimental traumatic brain injury: the role of excitatory amino acids in Hoff JTBetz AL (eds): Intracranial Pressure VII. Berlin: Springer1989 pp 584588Katayama Y Cheung MK Alves A et al: Ion fluxes and cell swelling in experimental traumatic brain injury: the role of excitatory amino acids in Hoff JT Betz AL (eds): Intracranial Pressure VII. Berlin: Springer 1989 pp 584–588

    • Search Google Scholar
    • Export Citation
  • 33.

    Kawamata TKatayama YHovda DAet al: Administration of excitatory amino acid antagonists via microdialysis attenuates the increase in glucose utilization seen following concussive brain injury. J Cereb Blood Flow Metab 12:12241992Kawamata T Katayama Y Hovda DA et al: 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 1992

    • Search Google Scholar
    • Export Citation
  • 34.

    Kipnis DMHelmreich ECori CF: Studies of tissue permeability. IV. The distribution of glucose between plasma and muscle. J Biol Chem 234:1651701959Kipnis DM Helmreich E Cori CF: Studies of tissue permeability. IV. The distribution of glucose between plasma and muscle. J Biol Chem 234:165–170 1959

    • Search Google Scholar
    • Export Citation
  • 35.

    Langfitt TWObrist WDAlavi Aet al: Computerized tomography, magnetic resonance imaging, and positron emission tomography in the study of brain trauma. Preliminary observations. J Neurosurg 64:7607671986Langfitt TW Obrist WD Alavi A et al: Computerized tomography magnetic resonance imaging and positron emission tomography in the study of brain trauma. Preliminary observations. J Neurosurg 64:760–767 1986

    • Search Google Scholar
    • Export Citation
  • 36.

    Lee SMHovda DABecker DP: Core of degenerating neurons in the ipsilateral parietal cortex induces spreading depression following a lateral fluid percussion brain injury. Soc Neurosci 20:8461994 (Abstract)Lee SM Hovda DA Becker DP: Core of degenerating neurons in the ipsilateral parietal cortex induces spreading depression following a lateral fluid percussion brain injury. Soc Neurosci 20:846 1994 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 37.

    Lewis LDLjunggren BNorberg Ket al: Changes in carbohydrate substrates, amino acids, and ammonia in the brain during insulin-induced hypoglycemia. J Neurochem 23:6596711974Lewis LD Ljunggren B Norberg K et al: Changes in carbohydrate substrates amino acids and ammonia in the brain during insulin-induced hypoglycemia. J Neurochem 23:659–671 1974

    • Search Google Scholar
    • Export Citation
  • 38.

    Lothman EWCollins RC: Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res 218:2993181981Lothman EW Collins RC: Kainic acid induced limbic seizures: metabolic behavioral electroencephalographic and neuropathological correlates. Brain Res 218:299–318 1981

    • Search Google Scholar
    • Export Citation
  • 39.

    Marion DWDarby JYonas H: Acute regional cerebral blood flow changes caused by severe head injuries. J Neurosurg 74:4074141991Marion DW Darby J Yonas H: Acute regional cerebral blood flow changes caused by severe head injuries. J Neurosurg 74:407–414 1991

    • Search Google Scholar
    • Export Citation
  • 40.

    Martin NADoberstein C: Cerebral blood flow measurement in neurosurgical intensive care. Neurosurg Clin North Am 5:6076181994Martin NA Doberstein C: Cerebral blood flow measurement in neurosurgical intensive care. Neurosurg Clin North Am 5:607–618 1994

    • Search Google Scholar
    • Export Citation
  • 41.

    Mayevsky ADoron ASalame Ket al: Multiparametric brain function analyzer—a breakthrough in patient monitoring and evaluation after traumatic head injury. J Neurotrauma 12:4491995 (Abstract)Mayevsky A Doron A Salame K et al: Multiparametric brain function analyzer—a breakthrough in patient monitoring and evaluation after traumatic head injury. J Neurotrauma 12:449 1995 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 42.

    Mazziotta JCPhelps ME: Positron emission tomography studies of the brain in Phelps MEMazziotta JCSchelbert HR (eds): Positron Emission Tomography and Autoradiography: Principles and Application for the Brain and Heart. New York: Raven Press1986 pp 493579Mazziotta JC Phelps ME: Positron emission tomography studies of the brain in Phelps ME Mazziotta JC Schelbert HR (eds): Positron Emission Tomography and Autoradiography: Principles and Application for the Brain and Heart. New York: Raven Press 1986 pp 493–579

    • Search Google Scholar
    • Export Citation
  • 43.

    McIlwain H: Phosphates of brain during in vitro metabolism: effects of oxygen, glucose, glutamate, glutamine, and calcium and potassium salts. Biochem J 52:2892951952McIlwain H: Phosphates of brain during in vitro metabolism: effects of oxygen glucose glutamate glutamine and calcium and potassium salts. Biochem J 52:289–295 1952

    • Search Google Scholar
    • Export Citation
  • 44.

    Muizelaar JP: Cerebral ischemia-reperfusion injury after severe head injury and its possible treatment with polyethyleneglycolsuperoxide dismutase. Ann Emerg Med 22:101410211993Muizelaar JP: Cerebral ischemia-reperfusion injury after severe head injury and its possible treatment with polyethyleneglycolsuperoxide dismutase. Ann Emerg Med 22:1014–1021 1993

    • Search Google Scholar
    • Export Citation
  • 45.

    Nakai HMatsuda HTakara Eet al: Changes in lumped and rate constants in experimental cerebral ischemia—intra-animal comparison before and after middle cerebral artery occlusion. Neurol Med Chir 28:11171988Nakai H Matsuda H Takara E et al: Changes in lumped and rate constants in experimental cerebral ischemia—intra-animal comparison before and after middle cerebral artery occlusion. Neurol Med Chir 28:11–17 1988

    • Search Google Scholar
    • Export Citation
  • 46.

    Nedergaard MAstrup J: Infarct rim: effect of hyperglycemia on direct current potential and [14C]2-deoxyglucose phosphorylation. J Cereb Blood Flow Metab 6:6076151986Nedergaard M Astrup J: Infarct rim: effect of hyperglycemia on direct current potential and [14C]2-deoxyglucose phosphorylation. J Cereb Blood Flow Metab 6:607–615 1986

    • Search Google Scholar
    • Export Citation
  • 47.

    Nedergaard MJakobsen JDiemer NH: Autoradiographic determination of cerebral glucose content, blood flow, and glucose utilization in focal ischemia of the rat brain: influence of the plasma glucose concentration. J Cereb Blood Flow Metab 8:1001081988Nedergaard M Jakobsen J Diemer NH: Autoradiographic determination of cerebral glucose content blood flow and glucose utilization in focal ischemia of the rat brain: influence of the plasma glucose concentration. J Cereb Blood Flow Metab 8:100–108 1988

    • Search Google Scholar
    • Export Citation
  • 48.

    Obrist WDLangfitt TWJaggi JLet al: Cerebral blood flow and metabolism in comatose patients with acute head injury. Relationship to intracranial hypertension. J Neurosurg 61:2412531984Obrist WD Langfitt TW Jaggi JL et al: Cerebral blood flow and metabolism in comatose patients with acute head injury. Relationship to intracranial hypertension. J Neurosurg 61:241–253 1984

    • Search Google Scholar
    • Export Citation
  • 49.

    Obrist WDThompson HK JrWang HSet al: Regional cerebral blood flow estimated by 133xenon inhalation. Stroke 6:2452561975Obrist WD Thompson HK Jr Wang HS et al: Regional cerebral blood flow estimated by 133xenon inhalation. Stroke 6:245–256 1975

    • Search Google Scholar
    • Export Citation
  • 50.

    Oldendorf WH: Brain uptake of radiolabeled amino acids, amines, and hexoses after arterial injection. Am J Physiol 221:162916391971Oldendorf WH: Brain uptake of radiolabeled amino acids amines and hexoses after arterial injection. Am J Physiol 221:1629–1639 1971

    • Search Google Scholar
    • Export Citation
  • 51.

    Persson LHillered L: Chemical monitoring of neurosurgical intensive care patients using intracerebral microdialysis. J Neurosurg 76:72801992Persson L Hillered L: Chemical monitoring of neurosurgical intensive care patients using intracerebral microdialysis. J Neurosurg 76:72–80 1992

    • Search Google Scholar
    • Export Citation
  • 52.

    Phelps MEHuang SCHoffman EJet al: Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: validation of method. Ann Neurol 6:3713881978Phelps ME Huang SC Hoffman EJ et al: Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: validation of method. Ann Neurol 6:371–388 1978

    • Search Google Scholar
    • Export Citation
  • 53.

    Rappaport ZHRansohoff JHass WK: Cerebral metabolism in head trauma. Prog Neurol Surg 10:1131981Rappaport ZH Ransohoff J Hass WK: Cerebral metabolism in head trauma. Prog Neurol Surg 10:1–13 1981

    • Search Google Scholar
    • Export Citation
  • 54.

    Robertson CSClifton GLGrossman RGet al: Alterations in cerebral availability of metabolic substrates after severe head injury. J Trauma 28:152315321988Robertson CS Clifton GL Grossman RG et al: Alterations in cerebral availability of metabolic substrates after severe head injury. J Trauma 28:1523–1532 1988

    • Search Google Scholar
    • Export Citation
  • 55.

    Robertson CSGrossman RGGoodman JCet al: The predictive value of cerebral anaerobic metabolism with cerebral infarction after head injury. J Neurosurg 67:3613681987Robertson CS Grossman RG Goodman JC et al: The predictive value of cerebral anaerobic metabolism with cerebral infarction after head injury. J Neurosurg 67:361–368 1987

    • Search Google Scholar
    • Export Citation
  • 56.

    Robinson PJRapoport SI: Glucose transport and metabolism in the brain. Am J Physiol 250:R127R1361986Robinson PJ Rapoport SI: Glucose transport and metabolism in the brain. Am J Physiol 250:R127–R136 1986

    • Search Google Scholar
    • Export Citation
  • 57.

    Ruff RMCrouch JATroster AIet al: Selected cases of poor outcome following a minor brain trauma: comparing neuropsychological and positron emission tomography assessment. Brain Injury 8:2973081994Ruff RM Crouch JA Troster AI et al: Selected cases of poor outcome following a minor brain trauma: comparing neuropsychological and positron emission tomography assessment. Brain Injury 8:297–308 1994

    • Search Google Scholar
    • Export Citation
  • 58.

    Shah KRWest M: The effect of concussion on cerebral uptake of 2-deoxy-D-glucose in rat. Neurosci Lett 40:2872911983Shah KR West M: The effect of concussion on cerebral uptake of 2-deoxy-D-glucose in rat. Neurosci Lett 40:287–291 1983

    • Search Google Scholar
    • Export Citation
  • 59.

    Shalmon EKelly DFBergsneider Met al: Human cerebral microdialysis: dynamic changes in EAA following severe brain injury. J Neurotrauma 12:1401995 (Abstract)Shalmon E Kelly DF Bergsneider M et al: Human cerebral microdialysis: dynamic changes in EAA following severe brain injury. J Neurotrauma 12:140 1995 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 60.

    Shapira YSetton DArtru AAet al: Blood-brain barrier permeability, cerebral edema, and neurologic function after closed head injury in rats. Anesth Analg 77:1411481993Shapira Y Setton D Artru AA et al: Blood-brain barrier permeability cerebral edema and neurologic function after closed head injury in rats. Anesth Analg 77:141–148 1993

    • Search Google Scholar
    • Export Citation
  • 61.

    Shinohara MDollinger BBrown Get al: Cerebral glucose utilization: local changes during and after recovery from spreading cortical depression. Science 203:1881901979Shinohara M Dollinger B Brown G et al: Cerebral glucose utilization: local changes during and after recovery from spreading cortical depression. Science 203:188–190 1979

    • Search Google Scholar
    • Export Citation
  • 62.

    Shiraishi KSharp FRSimon RP: Sequential metabolic changes in rat brain following middle cerebral artery occlusion; a 2-deoxyglucose study. J Cereb Blood Flow Metab 9:7657731989Shiraishi K Sharp FR Simon RP: Sequential metabolic changes in rat brain following middle cerebral artery occlusion; a 2-deoxyglucose study. J Cereb Blood Flow Metab 9:765–773 1989

    • Search Google Scholar
    • Export Citation
  • 63.

    Smith SLAndrus PKZhang JRet al: Direct measurement of hydroxyl radicals, lipid peroxidation, and blood-brain barrier disruption following unilateral cortical impact head injury in the rat. J Neurotrauma 11:3934041994Smith SL Andrus PK Zhang JR et al: Direct measurement of hydroxyl radicals lipid peroxidation and blood-brain barrier disruption following unilateral cortical impact head injury in the rat. J Neurotrauma 11:393–404 1994

    • Search Google Scholar
    • Export Citation
  • 64.

    Soares HDHicks RRSmith Det al: Inflammatory leukocyte recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J Neurosci 15:822382331995Soares HD Hicks RR Smith D et al: Inflammatory leukocyte recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J Neurosci 15:8223–8233 1995

    • Search Google Scholar
    • Export Citation
  • 65.

    Sunami KNakamura TKubota Met al: Spreading depression following experimental head injury in the rat. Neurol Med Chir 29:9759801989Sunami K Nakamura T Kubota M et al: Spreading depression following experimental head injury in the rat. Neurol Med Chir 29:975–980 1989

    • Search Google Scholar
    • Export Citation
  • 66.

    Sunami KNakamura TOzawa Yet al: Hypermetabolic state following experimental head injury. Neurosurg Rev 12:4004151989Sunami K Nakamura T Ozawa Y et al: Hypermetabolic state following experimental head injury. Neurosurg Rev 12:400–415 1989

    • Search Google Scholar
    • Export Citation
  • 67.

    Tabaddor KBhushan CPevsner PHet al: Prognostic value of cerebral blood flow (CBF) and cerebral metabolic rate of oxygen (CMRO2) in acute head trauma. J Trauma 12:105310551972Tabaddor K Bhushan C Pevsner PH et al: Prognostic value of cerebral blood flow (CBF) and cerebral metabolic rate of oxygen (CMRO2) in acute head trauma. J Trauma 12:1053–1055 1972

    • Search Google Scholar
    • Export Citation
  • 68.

    Talairach JTournoux P: Co-Planar Stereotaxic Atlas of the Human Brain. Stuttgart: Thieme1988 pp 84110Talairach J Tournoux P: Co-Planar Stereotaxic Atlas of the Human Brain. Stuttgart: Thieme 1988 pp 84–110

    • Search Google Scholar
    • Export Citation
  • 69.

    Tanno HNockels RPPitts LHet al: Breakdown of the blood-brain barrier after fluid percussion brain injury in the rat: Part 2: effect of hypoxia on permeability to plasma proteins. J Neurotrauma 9:3353471992Tanno H Nockels RP Pitts LH et al: Breakdown of the blood-brain barrier after fluid percussion brain injury in the rat: Part 2: effect of hypoxia on permeability to plasma proteins. J Neurotrauma 9:335–347 1992

    • Search Google Scholar
    • Export Citation
  • 70.

    Teasdale GJennett B: Assessment of coma and impaired consciousness. A practical scale. Lancet 2:81841974Teasdale G Jennett B: Assessment of coma and impaired consciousness. A practical scale. Lancet 2:81–84 1974

    • Search Google Scholar
    • Export Citation
  • 71.

    Tenjin HUeda SMizukawa Net al: Positron emission tomographic studies on cerebral hemodynamics in patients with cerebral contusion. Neurosurgery 26:9719791990Tenjin H Ueda S Mizukawa N et al: Positron emission tomographic studies on cerebral hemodynamics in patients with cerebral contusion. Neurosurgery 26:971–979 1990

    • Search Google Scholar
    • Export Citation
  • 72.

    Theodore WHNewmark MESato Set al: [18F]Fluorodeoxyglucose positron emission tomography in refractory complex partial seizures. Ann Neurol 14:4294371983Theodore WH Newmark ME Sato S et al: [18F]Fluorodeoxyglucose positron emission tomography in refractory complex partial seizures. Ann Neurol 14:429–437 1983

    • Search Google Scholar
    • Export Citation
  • 73.

    Todd NVGraham DI: Blood-brain barrier damage in traumatic brain contusions. Acta Neurochir Suppl 51:2962991990Todd NV Graham DI: Blood-brain barrier damage in traumatic brain contusions. Acta Neurochir Suppl 51:296–299 1990

    • Search Google Scholar
    • Export Citation
  • 74.

    Tommasino CGrana CLucignani Get al: Regional cerebral metabolism of glucose in comatose and vegetative state patients. J Neurosurg Anesthesiol 7:1091161995Tommasino C Grana C Lucignani G et al: Regional cerebral metabolism of glucose in comatose and vegetative state patients. J Neurosurg Anesthesiol 7:109–116 1995

    • Search Google Scholar
    • Export Citation
  • 75.

    Toulmond SDuval DSerrano Aet al: Biochemical and histological alterations induced by fluid percussion brain injury in the rat. Brain Res 620:24311993Toulmond S Duval D Serrano A et al: Biochemical and histological alterations induced by fluid percussion brain injury in the rat. Brain Res 620:24–31 1993

    • Search Google Scholar
    • Export Citation
  • 76.

    van den Brink WASantos BOMarmarou Aet al: Quantitative analysis of blood-brain barrier damage in two models of experimental head injury in the rat. Acta Neurochir Suppl 60:4564581994van den Brink WA Santos BO Marmarou A et al: Quantitative analysis of blood-brain barrier damage in two models of experimental head injury in the rat. Acta Neurochir Suppl 60:456–458 1994

    • Search Google Scholar
    • Export Citation
  • 77.

    Wise RJSRhodes CGGibbs JMet al: Disturbance of oxidative metabolism of glucose in recent human cerebral infarcts. Ann Neurol 14:6276371983Wise RJS Rhodes CG Gibbs JM et al: Disturbance of oxidative metabolism of glucose in recent human cerebral infarcts. Ann Neurol 14:627–637 1983

    • Search Google Scholar
    • Export Citation
  • 78.

    Yoshino AHovda DAKatayama Yet al: Hippocampal CA3 lesion prevents postconcussive metabolic dysfunction in CA1. J Cereb Blood Flow Metab 12:99610061992Yoshino A Hovda DA Katayama Y et al: Hippocampal CA3 lesion prevents postconcussive metabolic dysfunction in CA1. J Cereb Blood Flow Metab 12:996–1006 1992

    • Search Google Scholar
    • Export Citation
  • 79.

    Yoshino AHovda DAKawamata Tet al: Dynamic changes in local cerebral glucose utilization following cerebral concussion in rats: evidence of a hyper- and subsequent hypometabolic state. Brain Res 561:1061191991Yoshino A Hovda DA Kawamata T et al: Dynamic changes in local cerebral glucose utilization following cerebral concussion in rats: evidence of a hyper- and subsequent hypometabolic state. Brain Res 561:106–119 1991

    • Search Google Scholar
    • Export Citation
  • 80.

    Zane CJKhanna RMartin Net al: Patterns of cerebral blood flow and transcranial Doppler ultrasound velocities following head injury. J Neurosurg 76:399A1992 (Abstract)Zane CJ Khanna R Martin N et al: Patterns of cerebral blood flow and transcranial Doppler ultrasound velocities following head injury. J Neurosurg 76:399A 1992 (Abstract)

    • Search Google Scholar
    • Export Citation
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