brain injury; consciousness; FDG-PET; metabolism; minimally conscious state; vegetative state
Abstract :
[en] The differentiation of the vegetative or unresponsive wakefulness syndrome (VS/UWS) from the minimally conscious state (MCS) is
an important clinical issue. The cerebral metabolic rate of glucose (CMRglc) declines when consciousness is lost, and may reveal the
residual cognitive function of these patients. However, no quantitative comparisons of cerebral glucose metabolism in VS/UWS and
MCS have yet been reported. We calculated the regional and whole-brain CMRglc of 41 patients in the states of VS/UWS (n = 14),
MCS (n = 21) or emergence from MCS (EMCS, n = 6), and healthy volunteers (n = 29). Global cortical CMRglc in VS/UWS and MCS
averaged 42% and 55% of normal, respectively. Differences between VS/UWS and MCS were most pronounced in the frontoparietal
cortex, at 42% and 60% of normal. In brainstem and thalamus, metabolism declined equally in the two conditions. In EMCS,
metabolic rates were indistinguishable from those of MCS. Ordinal logistic regression predicted that patients are likely to emerge
into MCS at CMRglc above 45% of normal. Receiver-operating characteristics showed that patients in MCS and VS/UWS can be
differentiated with 82% accuracy, based on cortical metabolism. Together these results reveal a significant correlation between
whole-brain energy metabolism and level of consciousness, suggesting that quantitative values of CMRglc reveal consciousness in
severely brain-injured patients.
Research center :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurology
Author, co-author :
Stender, Johan
Kupers, Ron
Rodell, Anders
Thibaut, Aurore ; Université de Liège - ULiège > Centre de recherches du cyclotron
Chatelle, Camille ; Université de Liège - ULiège > Centre de recherches du cyclotron
Bruno, Marie-Aurélie ; Université de Liège - ULiège > Centre de recherches du cyclotron
Gejl, Michael
Bernard, Claire ; Université de Liège - ULiège > Département de physique > Département de physique
HUSTINX, Roland ; Centre Hospitalier Universitaire de Liège - CHU > Médecine nucléaire et imagerie oncologique
Laureys, Steven ; Université de Liège - ULiège > Centre de recherches du cyclotron
Gjedde, Albert
Language :
English
Title :
Quantitative rates of brain glucose metabolism distinguish minimally conscious from vegetative state patients
Medical aspects of the persistent vegetative state (1). The Multi-Society Task Force on PVS. N Engl J Med 1994; 330: 1499-1508.
Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58: 349-353.
Laureys S, Schiff ND. Coma and consciousness: paradigms (re)framed by neuroimaging. Neuroimage 2012; 61: 478-491.
Laureys S, Owen AM, Schiff ND. Brain function in coma, vegetative state, and related disorders. Lancet Neurol 2004; 3: 537-546.
Stender J, Gosseries O, Charland-Verville V, Vanhaudenhuyse A, Demertzi A, Chatelle C et al. Diagnostic precision of PET imaging and functional MRIin disorders of consciousness: a clinical validation study. Lancet 2014; 384: 514-522.
Levy DE, Sidtis JJ, Rottenberg DA, Jarden JO, Strother SC, Dhawan V et al. Differences in cerebral blood flow and glucose utilization in vegetative versus locked-in patients. Ann Neurol 1987; 22: 673-682.
Rudolf J, Ghaemi M, Ghaemi M, Haupt WF, Szelies B, Heiss WD. Cerebral glucose metabolism in acute and persistent vegetative state. J Neurosurg Anesthesiol 1999; 11: 17-24.
Tommasino C, Grana C, Lucignani G, Torri G, Fazio F. Regional cerebral metabolism of glucose in comatose and vegetative state patients. J Neurosurg Anesthesiol 1995; 7: 109-116.
Gjedde AH, Bauer WR, Wong DF. Neurokinetics: the dynamics of neurobiology in vivo. Springer: New York, USA, 2011.
Shulman RG, Hyder F, Rothman DL. Baseline brain energy supports the state of consciousness. Proc Natl Acad Sci USA 2009; 106:11096-11101
Hyder F, Fulbright RK, Shulman RG, Rothman DL. Glutamatergic function in the resting awake human brain is supported by uniformly high oxidative energy. J Cereb Blood Flow Metab 2013; 33:339-347
Demertzi A, Soddu A, Laureys S. Consciousness supporting networks. Curr Opin Neurobiol 2013; 23:239-244
Dehaene S, Changeux J-P. Experimental and theoretical approaches to conscious processing. Neuron 2011; 70:200-227
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ-F, Bruno M-A, Boveroux P, Schnakers C et al. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 2010; 133:161-171
Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 2007; 27:2349-2356
Vanhaudenhuyse A, Demertzi A, Schabus M, Noirhomme Q, Bredart S, Boly M et al. Two distinct neuronal networks mediate the awareness of environment and of self. J Cogn Neurosci 2011; 23:570-578
Giacino JT, Fins JJ, Laureys S, Schiff ND. Disorders of consciousness after acquired brain injury: the state of the science. Nat Rev Neurol 2014; 10:99-114
Thibaut A, Bruno M-A, Chatelle C, Gosseries O, Vanhaudenhuyse A, Demertzi A et al. Metabolic activity in external and internal awareness networks in severely brain-damaged patients. J Rehabil Med 2012; 44:487-494
Nakase-Richardson R, Yablon SA, Sherer M, Nick TG, Evans CC. Emergence from minimally conscious state: insights from evaluation of posttraumatic confusion. Neurology 2009; 73:1120-1126
Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004; 85:2020-2029
Seel RT, Sherer M, Whyte J, Katz DI, Giacino JT, Rosenbaum AM et al. Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. Arch Phys Med Rehabil 2010; 91:1795-1813
Sokoloff L, Reivich M, Kennedy C, Rosiers Des MH, Patlak CS, Pettigrew KD et al. 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 1977; 28:897-916
Takagi S, Takahashi W, Shinohara Y, Yasuda S, Ide M, Shohtsu A et al. Quantitative PET cerebral glucose metabolism estimates using a single non-arterialized venous-blood sample. Ann Nucl Med 2004; 18:297-302
Strauss LG, Pan L, Cheng C, Dimitrakopoulou-Strauss A. (18)F-Deoxyglucose (FDG) kinetics evaluated by a non-compartment model based on a linear regression function using a computer based simulation: correlation with the parameters of the two-tissue compartment model. Am J Nucl Med Mol Imaging 2012; 2:448-457
Kuwabara H, Gjedde A. Measurements of glucose phosphorylation with FDG and PET are not reduced by dephosphorylation of FDG-6-phosphate. J Nucl Med 1991; 32:692-698
Gjedde A. Positron Emission Tomography of Brain Glucose Metabolism with [18F] Fluorodeoxyglucose in Humans. In: Hirrlinger J, Waagepetersen H (eds). Brain Energy Metabolism, Neuromethods, Vol 90. Springer Science + Business Media: New York, 2014.
Darkner S, Sporring J. Locally orderless registration. IEEE Trans Pattern Anal Mach Intell 2013; 35:1437-1450
Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006; 31:968-980
Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG. Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci USA 1998; 95:316-321
Schlünzen L, Juul N, Hansen KV, Cold GE. Regional cerebral blood flow and glucose metabolism during propofol anaesthesia in healthy subjects studied with positron emission tomography. Acta Anaesthesiol Scand 2012; 56:248-255
Schlünzen L, Juul N, Hansen KV, Gjedde A, Cold GE. Regional cerebral glucose metabolism during sevoflurane anaesthesia in healthy subjects studied with positron emission tomography. Acta Anaesthesiol Scand 2010; 54:603-609
Alkire MT, Pomfrett CJ, Haier RJ, Gianzero MV, Chan CM, Jacobsen BP et al. Functional brain imaging during anesthesia in humans: effects of halothane on global and regional cerebral glucose metabolism. Anesthesiology 1999; 90:701-709
Maquet P. Functional neuroimaging of normal human sleep by positron emission tomography. J Sleep Res 2000; 9:207-231
Kotchoubey B, Merz S, Lang S, Markl A, Müller F, Yu T et al. Global functional connectivity reveals highly significant differences between the vegetative and the minimally conscious state. J Neurol 2013; 260:975-983
White NS, Alkire MT. Impaired thalamocortical connectivity in humans during general-anesthetic-induced unconsciousness. Neuroimage 2003; 19:402-411
Laureys S, Faymonville ME, Luxen A, Lamy M, Franck G, Maquet P. Restoration of thalamocortical connectivity after recovery from persistent vegetative state. Lancet 2000; 355:1790-1791
Boly M, Garrido MI, Gosseries O, Bruno M-A, Boveroux P, Schnakers C et al. Preserved feedforward but impaired top-down processes in the vegetative state. Science 2011; 332:858-862
Maandag NJG, Coman D, Sanganahalli BG, Herman P, Smith AJ, Blumenfeld H et al. Energetics of neuronal signaling and fMRI activity. Proc Natl Acad Sci USA 2007; 104:20546-20551
Goldfine AM, Victor JD, Conte MM, Bardin JC, Schiff ND. Determination of awareness in patients with severe brain injury using EEG power spectral analysis. Clin Neurophysiol 2011; 122:2157-2168
Lechinger J, Bothe K, Pichler G, Michitsch G, Donis J, Klimesch W et al. CRS-R score in disorders of consciousness is strongly related to spectral EEG at rest. J Neurol 2013; 260:2348-2356
King J-R, Sitt JD, Faugeras F, Rohaut B, Karoui El I, Cohen L et al. Information sharing in the brain indexes consciousness in noncommunicative patients. Curr Biol 2013; 23:1914-1919
Silva S, Alacoque X, Fourcade O, Samii K, Marque P, Woods R et al. Wakefulness and loss of awareness: brain and brainstem interaction in the vegetative state. Neurology 2010; 74:313-320
Långsjö JW, Alkire MT, Kaskinoro K, Hayama H, Maksimow A, Kaisti KK et al. Returning from oblivion: imaging the neural core of consciousness. J Neurosci 2012; 32:4935-4943
Vogt BA, Laureys S. Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. Prog Brain Res 2005; 150:205-217
Voss HU. Possible axonal regrowth in late recovery from the minimally conscious state. J Clin Invest 2006; 116:2005-2011
Fernández-Espejo D, Junque C, Bernabeu M, Roig-Rovira T, Vendrell P, Mercader JM. Reductions of thalamic volume and regional shape changes in the vegetative and the minimally conscious states. J Neurotrauma 2010; 27:1187-1193
Adams JH, Graham DI, Jennett B. The neuropathology of the vegetative state after an acute brain insult. Brain 2000; 123(Pt 7):1327-1338
Schiff ND, Giacino JT, Kalmar K, Victor JD, Baker K, Gerber M et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 2007; 448:600-603
Llinás R, Ribary U, Contreras D, Pedroarena C. The neuronal basis for consciousness. Philos Trans R Soc Lond B Biol Sci 1998; 353:1841-1849
Schiff ND, Ribary U, Moreno DR, Beattie B, Kronberg E, Blasberg R et al. Residual cerebral activity and behavioural fragments can remain in the persistently vegetative brain. Brain 2002; 125:1210-1234