Anisotropy; Aspartic Acid/analogs & derivatives/metabolism; Brain Mapping; Choline/metabolism; Coma/diagnosis/metabolism/physiopathology; Creatine/metabolism; Databases, Factual/statistics & numerical data; Diffusion Magnetic Resonance Imaging/methods; Humans; Image Processing, Computer-Assisted/methods; Magnetic Resonance Spectroscopy/methods; Protons/diagnostic use; Recovery of Function/physiology; Severity of Illness Index; Survivors/statistics & numerical data
Abstract :
[en] The status of comatose patient is currently established on the basis of the patient-exhibited behaviors. Clinical assessment is subjective and, in 40% of patients, fails to distinguish vegetative state (VS) from minimally conscious states (MCS). The technologic advances of magnetic resonance imaging (MRI) have dramatically improved our understanding of these altered states of consciousness. The role of neuroimaging in coma survivors has increased beyond the simple evaluation of morphological abnormalities. The development of 1H-MR spectroscopy (MRS) and diffusion tensor imaging (DTI) provide opportunity to evaluate processes that cannot be approached by current morphologic MRI sequences. They offer potentially unique insights into the histopathology of VS and MCS. The MRS is a powerful noninvasive imaging technique that enables the in vivo quantification of certain chemical compound or metabolites as N-acetylaspartate (NAA), Choline (Cho), and Creatine (Cr). These biomarkers explore neuronal integrity (NAA), cell membrane turnover (Cho), and cell energetic function (Cr). DTI is an effective and proved quantitative method for evaluating tissue integrity at microscopic level. It provides information about the microstructure and the architecture of tissues, especially the white matter. Various physical parameters can be extracted from this sequence: the fractional anisotropy (FA), a marker of white matter integrity; mean diffusivity (MD); and the apparent diffusion coefficient (ADC) which can differentiate cytotoxic and vasogenic edema. The most prominent findings with MRS and DTI performed in traumatic brain-injured (TBI) patients in subacute phase are the reduction of the NAA/Cr ratio in posterior pons and the decrease of mean infratentorial and supratentorial FA except in posterior pons that enables to predict unfavorable outcome at 1 year from TBI with up to 86% sensitivity and 97% specificity. This review will focus on the interest of comatose patients MRI multimodal assessment with MRS and DTI. It will emphasize the advantages and pitfalls of these techniques in particular in predicting the coma survivors' outcome.
Disciplines :
Neurology
Author, co-author :
TSHIBANDA, Luaba ; Centre Hospitalier Universitaire de Liège - CHU > Imagerie médicale
Adams J.H., Graham D.I., Murray L.S., and Scott G. Diffuse axonal injury due to nonmissile head injury in humans: An analysis of 45 cases. Annals of Neurology 12 (1982) 557-563
Anderson C.V., Wood D.M., Bigler E.D., and Blatter D.D. Lesion volume, injury severity, and thalamic integrity following head injury. Journal of Neurotrauma 13 (1996) 59-65
Andrews K., Murphy L., Munday R., and Littlewood C. Misdiagnosis of the vegetative state: Retrospective study in a rehabilitation unit. British Medical Journal 313 7048 (1996) 13-16
Arfanakis K., Haughton V.M., Carew J.D., Rogers B.P., Dempsey R.J., and Meyerand M.E. Diffusion tensor MR imaging in diffuse axonal injury. American Journal of Neuroradiology 23 (2002) 794-802
Assaf Y., and Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: A review. Journal of Molecule Neuroscience 34 (2008) 51-61
Baslow M.H., Hrabe J., and Guilfoyle D.N. Dynamic relationship between neurostimulation and N-acetylaspartate metabolism in the human visual cortex: Evidence that NAA functions as a molecular water pump during visual stimulation. Journal of Molecule Neuroscience 32 (2007) 235-245
Baslow M.H., Suckow R.F., Gaynor K., Bhakoo K.K., Marks N., Saito M., et al. Brain damage results in down-regulation of N-acetylaspartate as a neuronal osmolyte. Neuromolecular Medicine 3 (2003) 95-104
Beuthien-Baumann B., Handrick W., Schmidt T., Burchert W., Oehme L., Kropp J., et al. Persistent vegetative state: Evaluation of brain metabolism and brain perfusion with PET and SPECT. Nuclear Medicine Communications 24 (2003) 643-649
Boly M., Faymonville M.E., Schnakers C., Peigneux P., Lambermont B., Phillips C., et al. Perception of pain in the minimally conscious state with PET activation: An observational study. Lancet Neurology 7 11 (2008) 1013-1020
Boly M., Phillips C., Tshibanda L., Vanhaudenhuyse A., Schabus M., Dang-Vu T.T., et al. Intrinsic brain activity in altered states of consciousness. How conscious is the default mode of brain function?. Annals of the New York Academy of Sciences 1129 (2008) 119-129
Carpentier A., Galanaud D., Puybasset L., Muller J.C., Lescot T., Boch A.L., et al. Early morphologic and spectroscopic magnetic resonance in severe traumatic brain injuries can detect "invisible brain stem damage" and predict "vegetative states". Journal of Neurotrauma 23 (2006) 674-685
Castillo M., Kwock L., and Mukherji S.K. Clinical applications of proton MR spectroscopy. American Journal of Neuroradiology 17 (1996) 1-15
Cecil K.M., Hills E.C., Sandel M.E., Smith D.H., McIntosh T.K., Mannon L.J., et al. Proton magnetic resonance spectroscopy for detection of axonal injury in the splenium of the corpus callosum of brain-injured patients. Journal of Neurosurgery 88 (1998) 795-801
Celesia G. Persistent vegetative state. Neurology 43 (1993) 1457-1458
Chan Y.L., Chu W.C., Wong G.W., and Yeung D.K. Diffusion-weighted MRI in shaken baby syndrome. Pediatric Radiology 33 (2003) 574-577
Childs N.L., and Mercer W.N. Misdiagnosing the persistent vegetative state. Misdiagnosis certainly occurs. British Medical Journal 313 7062 (1996) 944
Choe B.Y., Suh T.S., Choi K.H., Shinn K.S., Park C.K., and Kang J.K. Neuronal dysfunction in patients with closed head injury evaluated by in vivo 1H magnetic resonance spectroscopy. Investigative Radiology 30 (1995) 502-506
Cohen B.A., Inglese M., Rusinek H., Babb J.S., Grossman R.I., and Gonen O. Proton MR spectroscopy and MRI-volumetry in mild traumatic brain injury. American Journal of Neuroradiology 28 (2007) 907-913
Coleman M.R., Rodd J.M., Davis M.H., Johnsrude I.S., Menon D.K., Pickard J.D., et al. Do vegetative patients retain aspects of language comprehension? Evidence from fMRI. Brain 130 (2007) 2494-2507
Cox I.J. Development and applications of in vivo clinical magnetic resonance spectroscopy. Progress in Biophysics and Molecular Biology 65 (1996) 45-81
Danielsen E.R., and Ross B. Magnetic resonance spectroscopy diagnosis of neurological diseases. 1st ed. (1999), Marcel Dekker, Inc, New York
Ebisu T., Rooney W.D., Graham S.H., Weiner M.W., and Maudsley A.A. N-acetylaspartate as an in vivo marker of neuronal viability in kainate-induced status epilepticus: 1H magnetic resonance spectroscopic imaging. Journal of Cerebral Blood Flow & Metabolism 14 (1994) 373-382
Firsching R., Woischneck D., Diedrich M., Klein S., Ruckert A., Wittig H., et al. Early magnetic resonance imaging of brainstem lesions after severe head injury. Journal of Neurosurgery 89 (1998) 707-712
Friedman S., Brooks W., Jung R., Chiulli S., Sloan J., Montoya B., et al. Quantitative proton MRS predicts outcome after traumatic brain injury. Neurology 52 (1999) 1384-1391
Gale S.D., Johnson S.C., Bigler E.D., and Blatter D.D. Trauma-induced degenerative changes in brain injury: A morphometric analysis of three patients with preinjury and postinjury MR scans. Journal of Neurotrauma 12 (1995) 151-158
Garnett M.R., Blamire A.M., Corkill R.G., Cadoux-Hudson T.A., Rajagopalan B., and Styles P. Early proton magnetic resonance spectroscopy in normal-appearing brain correlates with outcome in patients following traumatic brain injury. Brain 123 (2000) 2046-2054
Gean A.D. White matter shearing injury and brainstem injury (1994), Raven, New York
Gentry L.R., Godersky J.C., Thompson B., and Dunn V.D. Prospective comparative study of intermediate-field MR and CT in the evaluation of closed head trauma. American Journal of Roentgenology 150 (1988) 673-682
Gerber D.J., Weintraub A.H., Cusick C.P., Ricci P., and Whiteneck G.G. Magnetic resonance imaging of traumatic brain injury: Relationship of T2*SE and T2GE to clinical severity and outcome. Brain Injury 18 (2004) 1083-1097
Hoelper B.M., Soldner F., Chone L., and Wallenfang T. Effect of intracerebral lesions detected in early MRI on outcome after acute brain injury. Acta Neurochirurgica. Supplement 76 (2000) 265-267
Holshouser B.A., Tong K.A., Ashwal S., Oyoyo U., Ghamsary M., Saunders D., et al. Prospective longitudinal proton magnetic resonance spectroscopic imaging in adult traumatic brain injury. Journal of Magnetic Resonance Imaging 24 (2006) 33-40
Huisman T., Sorensen A., Hergan K., Gonzalez R., and Schaefer P. Diffusion-weighted imaging for the evaluation of diffuse axonal injury in closed head injury. Journal of Computer Assisted Tomography 27 (2003) 5-11
Huisman T.A., Schwamm L.H., Schaefer P.W., Koroshetz W.J., Shetty-Alva N., Ozsunar Y., et al. Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. American Journal of Neuroradiology 25 (2004) 370-376
Jennett B. 30 years of the vegetative state: Clinical, ethical and legal problems. In: Laureys S. (Ed). The boundaries of consciousness: Neurobiology and neuropathology Vol. 150 (2005), Elsevier, Amsterdam 541-548
Jennett B., and Bond M. Assessment of outcome after severe brain damage. Lancet 7905 (1975) 480-484
Kampfl A., Schmutzhard E., Franz G., Pfausler B., Haring H.P., Ulmer H., et al. Prediction of recovery from post-traumatic vegetative state with cerebral magnetic-resonance imaging. Lancet 351 (1998) 1763-1767
Katz D. Traumatic brain injury (1997), Blackwell Science, Malden
Kelly A.B., Zimmerman R.D., Snow R.B., Gandy S.E., Heier L.A., and Deck M.D.F. Head trauma: Comparison of MR and CT-experience in 100 patients. American Journal of Neuroradiology 9 (1988) 699-708
Laureys S., Goldman S., Phillips C., Van Bogaert P., Aerts J., Luxen A., et al. Impaired effective cortical connectivity in vegetative state. Neuroimage 9 (1999) 377-382
Lewine J.D., Davis J.T., Sloan J.H., Kodituwakku P.W., and Orrison Jr. W.W. Neuromagnetic assessment of pathophysiologic brain activity induced by minor head trauma. American Journal of Neuroradiology 20 (1999) 857-866
Liu A.Y., Maldjian J.A., Bagley L.J., Sinson G.P., and Grossman R.I. Traumatic brain injury: Diffusion-weighted MR imaging findings. American Journal of Neuroradiology 20 (1999) 1636-1641
Marino S., Zei E., Battaglini M., Vittori C., Buscalferri A., Bramanti P., et al. Acute metabolic brain changes following traumatic brain injury and their relevance to clinical severity and outcome. Jounral of Neurology, Neurosurgery and Psychiatry 78 (2007) 501-507
Melhem E.R., Itoh R., Jones L., and Barker P.B. Diffusion tensor MR imaging of the brain: Effect of diffusion weighting on trace and anisotropy measurements. American Journal of Neuroradiology 21 (2000) 1813-1820
Moffett J.R., Ross B., Arun P., Madhavarao C.N., and Namboodiri A.M. N-Acetylaspartate in the CNS: From neurodiagnostics to neurobiology. Progress in Neurobiology 81 (2007) 89-131
Monti M.M., Coleman M.R., and Owen A.M. Neuroimaging and the vegetative state: Resolving the behavioral assessment dilemma?. Annals of the New York Academy of Sciences 1157 March (2009) 81-89
Murray J.G., Gean A.D., and Evans S.J. Imaging of acute head injury. Seminars in Ultrasound, CT and MRI 17 (1996) 185-205
Owen A.M., Coleman M.R., Boly M., Davis M.H., Laureys S., and Pickard J.D. Detecting awareness in the vegetative state. Science 13 (2006) 1402
Parvizi J., and Damasio A. Consciousness and the brainstem. Cognition 79 (2001) 135-160
Paterakis K., Karantanas A.H., Komnos A., and Volikas Z. Outcome of patients with diffuse axonal injury: The significance and prognostic value of MRI in the acute phase. Journal of Trauma 49 (2000) 1071-1075
Payne K., Taylor R.M., Stocking C., and Sachs G.A. Physicians' attitudes about the care of patients in the persistent vegetative state: A national survey. Annals of Internal Medicine 125 (1996) 104-110
Perlbarg, V., Puybasset, L., Tollard, E., Lehéricy, S., Benali, H., & Galanaud, D. (2009). Relation between brain lesion location and clinical outcome in patients with severe traumatic brain injury: A diffusion tensor imaging study using voxel-based approaches. Human Brain Mapping (in press).
Pierallini A., Pantano P., Fantozzi L.M., Bonamini M., Vichi R., Zylberman R., et al. Correlation between MRI findings and long-term outcome in patients with severe brain trauma. Neuroradiology 42 (2000) 860-867
Pierpaoli C., Jezzard P., Basser P.J., Barnett A., and Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology 201 (1996) 637-648
Plum F., and Posner J. The diagnosis of stupor and coma. 3rd ed. (1980), Oxford University Press, Oxford, UK
Pouwels P.J., and Frahm J. Regional metabolite concentrations in human brain as determined by quantitative localized proton MRS. Magnetic Resonance Medicine 39 (1998) 53-60
Ricci R., Barbarella G., Musi P., Boldrini P., Trevisan C., and Basaglia N. Localised proton MR spectroscopy of brain metabolism changes in vegetative patients. Neuroradiology (1997) 313-319
Ross B., and Michaelis T. Clinical applications of magnetic resonance spectroscopy. Magnetic Resonance Quarterly 10 (1994) 191-247
Ross B.D., Ernst T., Kreis R., Haseler L.J., Bayer S., Danielsen E., et al. 1H MRS in acute traumatic brain injury. Journal of Magnetic Resonance Imaging 8 (1998) 829-840
Salmond C.H., Menon D.K., Chatfield D.A., Williams G.B., Pena A., Sahakian B.J., et al. Diffusion tensor imaging in chronic head injury survivors: Correlations with learning and memory indices. Neuroimage 29 (2006) 117-124
Schaefer P.W., Huisman T.A.G., Sorensen A.G., Gonzalez R.G., and Schwamm L.H. Diffusion-weighted MR imaging in closed head injury: High correlation with initial Glasgow Coma Scale score and score on Modified Ranking Scale at Discharge. Radiology 233 1 (2004) 58-66
Scheid R., Preul C., Gruber O., Wiggins C., and von Cramon D.Y. Diffuse axonal injury associated with chronic traumatic brain injury: Evidence from T2*-weighted gradient-echo imaging at 3 T. American Journal of Neuroradiology 24 (2003) 1049-1056
Schnakers C., Vanhaudenhuyse A., Giacino J., Ventura M., Boly M., Majerus S., et al. Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment. BMC Neurology 21 9 (2009) 35
Selden N., Gitelman D., Salamon-Murayama N., Parrish T., and Mesulam M. Trajectories of cholinergic pathways within the cerebral hemispheres of the human brain. Brain 121 (1998) 2249-2257
Shanmuganathan K., Gullapalli R.P., Mirvis S.E., Roys S., and Murthy P. Whole-brain apparent diffusion coefficient in traumatic brain injury: Correlation with Glasgow Coma Scale. American Jounral of Neuroradiogy 25 (2004) 539-544
Signoretti S., Marmarou A., Fatouros P., Hoyle R., Beaumont A., Sawauchi S., et al. Application of chemical shift imaging for measurement of NAA in head injured patients. Acta Neurochirurgica. Supplement 81 (2002) 373-375
Sinson G., Bagley L.J., Cecil K.M., Torchia M., McGowan J.C., Lenkinski R.E., et al. Magnetization transfer imaging and proton MR spectroscopy in the evaluation of axonal injury: Correlation with clinical outcome after traumatic brain injury. American Journal Neuroradiology 22 (2001) 143-151
Strich S.J. Shearing of nerve fibres as a cause of brain damage due to head injury: A pathological study of twenty cases. Lancet 2 (1961) 443-448
Sullivan E.V., Adalsteinsson E., Spielman D.M., Hurd R.E., and Pfefferbaum A. N-acetylaspartate - A marker of neuronal integrity. Annals of Neurology 50 (2001) 824-825
Tollard E., Galanaud D., Perlbarg V., Sanchez-Pena P., Le Fur Y., Abdennour L., et al. Experience of diffusion tensor imaging and 1H spectroscopy for outcome prediction in severe traumatic brain injury: Preliminary results. Critical Care Medicine 37 (2009) 1448-1455
Trivedi M.A., Ward M.A., Hess T.M., Gale S.D., Dempsey R.J., Rowley H.A., et al. Longitudinal changes in global brain volume between 79 and 409 days after traumatic brain injury: Relationship with duration of coma. Journal of Neurotrauma 24 5 (2007) 766-771
Uzan M., Albayram S., Dashti S.G., Aydin S., Hanci M., and Kuday C. Thalamic proton magnetic resonance spectroscopy in vegetative state induced by traumatic brain injury. Journal of Neurolology, Neurosurgery and Psychiatry 74 (2003) 33-38
Voss H.U., Uluç A.M., Dyke J.P., Watts R., Kobylarz E.J., McCandliss B.D., et al. Possible axonal regrowth in late recovery from the minimally conscious state. The Journal of Clinical Investigation 116 7 (2006) 1823-1825
Wedekind C., Fischbach R., Pakos P., Terhaag D., and Klug N. Comparative use of magnetic resonance imaging and electrophysiologic investigation for the prognosis of head injury. Journal of Trauma 47 (1999) 44-49
Weiss N., Galanaud D., Carpentier A., Naccache L., and Puybasset L. Clinical review: Prognostic value of magnetic resonance imaging in acute brain injury and coma. Critical Care 11 (2007) 230
Wood S.J., Berger G., Velakoulis D., Phillips L.J., McGorry P.D., Yung A.R., et al. Proton magnetic resonance spectroscopy in first episode psychosis and ultra high-risk individuals. Schizophrenia Bulletin 29 (2003) 831-843
Xu J., Rasmussen I.A., Lagopoulos J., and Haberg A. Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. Journal of Neurotrauma 24 (2007) 753-765
Yanagawa Y., Tsushima Y., Tokumaru A., Un-no Y., Sakamoto T., Okada Y., et al. A quantitative analysis of head injury using T2*-weighted gradient-echo imaging. Journal of Trauma 49 (2000) 272-277