Skip to main content Accessibility help
Hostname: page-component-66d7dfc8f5-cdn8t Total loading time: 0.761 Render date: 2023-02-08T08:57:19.696Z Has data issue: true Feature Flags: { "useRatesEcommerce": false } hasContentIssue true

10 - MRS in traumatic brain injury

Published online by Cambridge University Press:  04 August 2010

Peter B. Barker
The Johns Hopkins University School of Medicine
Alberto Bizzi
Istituto Neurologico Carlo Besta, Milan
Nicola De Stefano
Università degli Studi, Siena
Rao Gullapalli
University of Maryland, Baltimore
Doris D. M. Lin
The Johns Hopkins University School of Medicine
Get access


Key points

  • TBI is a major cause of morbidity in young adults and children.

  • Low levels of NAA and, if seen, increased lactate, in the early stage of injury are prognostic of poor outcome.

  • Other common metabolic abnormalities in TBI (most of which also correlate with poor outcome) include increased levels of choline, myo-inositol, and glutamate plus glutamine.

  • Metabolic abnormalities are observed with MRS in regions of the brain with normal appearance in conventional MRI.

  • MRI and MRS are difficult to perform in acutely ill TBI patients: MRS may be more feasible in mild TBI patients for the purpose of predicting long-term cognitive deficits.

  • The role of MRS in guiding TBI therapy is unknown.

  • The comparative value of MRS compared to other advanced imaging modalities remains to be determined.


Traumatic brain injury (TBI) is a leading cause of death and lifelong disability among children and young adults across the developed world. TBI is estimated to result in greater than $60 billion in direct and indirect annual costs due to health care and work loss disability. The Centers for Disease Control and Prevention (CDC) estimate that each year approximately 1.4 million Americans survive a TBI, among whom approximately 235,000 are hospitalized. Approximately 80,500 new TBI survivors are left each year with residual deficits consequent to their injury, which lead to long-term disabilities that may or may not be improved through rehabilitation. In 2001, 157,708 people died from acute traumatic injury, which accounted for about 6.5% of all deaths in the United States.

Clinical MR Spectroscopy
Techniques and Applications
, pp. 161 - 179
Publisher: Cambridge University Press
Print publication year: 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Finkelstein, E, Corso, P, Miller, T. The Incidence and Economic Burden of Injuries in the United States. New York (NY): Oxford University Press, 2006.CrossRefGoogle Scholar
Langlois, JA, Rutland-Brown, W, Thomas, KE. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations, and Deaths. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control, 2004.Google Scholar
,National Institute of Neurological Disorders and Stroke. Traumatic Brain Injury: Hope Through Research. Bethesda, MD: National Institutes of Health; Feb. NIH Publication No.: 02–158, 2002.
Thurman, D, Alverson, C, Dunn, K, Guerrero, J, Sniezek, J. Traumatic brain injury in the United States: A public health perspective. J Head Trauma Rehabil 1999; 14: 602–15.CrossRefGoogle ScholarPubMed
Ommaya, AK, Gennarelli, TA. Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries. Brain 1974; 97: 633–54.CrossRefGoogle ScholarPubMed
Ommaya, AK, Goldsmith, W, Thibault, L. Biomechanics and neuropathology of adult and pediatric head injury. Br J Neurosurg 2002; 16: 220–42.CrossRefGoogle Scholar
Povlishock, J, Becker, DP, Cheng, CL, Vaughan, GW. Axonal change in minor head injury. J Neuropathol Exp Neurol 1983; 42: 225–42.CrossRefGoogle ScholarPubMed
Elson, LM, Ward, CC. Mechanisms and pathophysiology of mild head injury. Semin Neurol 1994; 14: 8–18.CrossRefGoogle ScholarPubMed
McCrory, P, Johnston, KM, Mohtadi, NG, Meeuwisse, W. Evidence-based review of sport-related concussion: Basic science. Clin J Sport Med 2001; 11: 160–5.CrossRefGoogle ScholarPubMed
Johnston, KM, McCrory, P, Mohtadi, NG, Meeuwisse, W. Evidence-based review of sport-related concussion: Clinical science. Clin J Sport Med 2001; 11: 150–9.CrossRefGoogle ScholarPubMed
Graham, DI. Neuropathology of head injury. In Neurotrauma, Narayan, RK, Wilberger, JE, Povlishock, JT, Eds. Philadelphia: W. B. Saunders; 1996: 43–60.Google Scholar
Graham, DI, Gennarelli, TA, McIntosh, TK. Trauma. In Greenfield's Neuropathology, 7th edn, Graham, DJ, Lantos, PL, Eds. London: Arnold Press, 2002.Google Scholar
Gentry, LR. Imaging of closed head injury. Radiology 1994; 191: 1–17.CrossRefGoogle ScholarPubMed
DeKosky, ST, Kochanek, PM, Clark, RS, Ciallella, JR, Dixon, CE. Secondary injury after head trauma: Subacute and long-term mechanisms. Semin Clin Neuropsychiatry 1998; 3: 176–85.Google ScholarPubMed
Gorman, LK, Fu, K, Hovda, DA, Murray, M, Traystman, RJ. Effects of traumatic brain injury on the cholinergic system in the rat. J Neurotrauma 1996; 13: 457–63.CrossRefGoogle ScholarPubMed
Pike, BR, Hamm, RJ. Activating the post-traumatic cholinergic system for the treatment of cognitive impairment following traumatic brain injury. Pharmacol Biochem Behav 1997; 57: 785–91.CrossRefGoogle Scholar
Globus, MY, Alonso, O, Dietrich, WD, Busto, R, Ginsberg, MD. Glutamate release and free radical production following brain injury: Effects of posttraumatic hypothermia. J Neurochem 1995; 65: 1704–11.CrossRefGoogle ScholarPubMed
LaPlaca, MC, Lee, VM, Thibault, . An in vitro model of traumatic neuronal injury: Loading rate-dependent changes in acute cytosolic calcium and lactate dehydrogenase release. J Neurotrauma 1997; 14: 355–68.CrossRefGoogle Scholar
Farooqui, AA, Horrocks, . Lipid peroxides in the free radical pathophysiology of brain diseases. Cell Mol Neurobiol 1998; 18: 599–608.CrossRefGoogle ScholarPubMed
Nemetz, PN, Leibson, C, Naessens, JM, Beard, M, Kokmen, E, Annegers, JF, et al. Traumatic brain injury and time to onset of Alzheimer's disease: A population-based study. Am J Epidemiol 1999; 149: 32–40.CrossRefGoogle ScholarPubMed
Lye, TC, Shores, EA. Traumatic brain injury as a risk factor for Alzheimer's disease: A review. Neuropsychol Rev 2000; 10: 115–29.CrossRefGoogle ScholarPubMed
Chaumet, G, Quera-Salva, MA, Macleod, A, Hartley, S, Taillard, J, Sagaspe, Pet al. Is there a link between alertness and fatigue in patients with traumatic brain injury?Neurology 2008; 71: 1609–13.CrossRefGoogle Scholar
Makley, MJ, English, JB, Drubach, DA, Kreuz, AJ, Celnik, PA, Tarwater, PM.Prevalence of sleep disturbance in closed head injury patients in a rehabilitation unit. Neurorehabil Neural Repair 2008; 22: 341–7.CrossRefGoogle Scholar
Nampiaparampil, . Prevalence of chronic pain after traumatic brain injury: A systematic review. J Am Med Assoc 2008; 300: 711–9.CrossRefGoogle ScholarPubMed
Immonen, RJ, Kharatishvili, I, Gröhn, H, Pitkänen, A, Gröhn, OH. Quantitative MRI predicts long-term structural and functional outcome after experimental traumatic brain injury. NeuroImage 2008 [Epub ahead of print].
Menzel, JC. Depression in the elderly after traumatic brain injury: A systematic review. Brain Inj 2008; 22: 375–80.CrossRefGoogle ScholarPubMed
Muscara, F, Catroppa, C, Anderson, V. The impact of injury severity on executive function 7–10 years following pediatric traumatic brain injury. Dev Neuropsychol 2008; 33: 623–36.CrossRefGoogle ScholarPubMed
Nybo, T, Koskiniemi, M. Cognitive indicators of vocational outcome after severe traumatic brain injury (TBI) in childhood. Brain Inj 1999; 13: 759–66.Google ScholarPubMed
Adelson, PD, Kochanek, PN. Head injury in children. Child Neurol 1998; 13: 3–15.CrossRefGoogle ScholarPubMed
Kochanek, PM, Clark, RS, Ruppel, RA, Adelson, PD, Bell, MJ, Whalen, MJ, et al. Biochemical, cellular, and molecular mechanisms in the evolution of secondary damage after severe traumatic brain injury in infants and children. Lessons learned from the bedside. Pediatr Crit Care Med 2000; 1: 4–19.CrossRefGoogle Scholar
Levin, HS, Aldrich, EF, Saydjari, C, Eisenberg, HM, Foulkes, MA, Bellefleur, M, et al. Severe head injury in children: Experience of the Traumatic Coma Data Bank. Neurosurgery 1992; 31: 435–44.CrossRefGoogle ScholarPubMed
Garthe, E, States, JD, Mango, NK. Abbreviated injury scale unification: The case for a unified injury system for global use. J Trauma 1999; 47: 309–23.CrossRefGoogle ScholarPubMed
Teasdale, G, Jennett, B. Assessment of coma and impaired consciousness: A practical scale. Lancet 1974; 13: 81–3.CrossRefGoogle Scholar
Zimmerman, RA. Craniocerebral trauma. In Cranial MRI and CT, 4th edn, Lee, SH, Rao, KCVG, Zimmerman, RA, Eds. New York: McGraw-Hill; 1999: 413–52.Google Scholar
Schunk, JE, Rodgerson, JD, Woodward, GA. The utility of head computed tomographic scanning in pediatric patients with normal neurologic examination in the emergency department. Pediatr Emerg Care 1996; 12: 160–5.CrossRefGoogle ScholarPubMed
Cihangiroglu, M, Ramsey, RG, Drohmann, GJ. Brain injury: Analysis of imaging modalities. Neurol Res 2002; 24: 7–18.CrossRefGoogle ScholarPubMed
Zee, CS, Go, J. CT of head trauma. Neuroimaging Clin N Am 1998; 8: 541–8.Google ScholarPubMed
Borzcuk, P. Mild head trauma. Emerg Med Clin North Am 1997; 15: 563.Google Scholar
Sojka, P, Stalnacke, BM. Normal findings by computer tomography do not exclude CNS injury. Lakartidningen 1999; 96: 616.Google Scholar
Gentry, LR. Head Trauma. Magnetic Resonance Imaging of the Brain and Spine (3rd edn), Atlas Ed, SW. Philadelphia: Lippincott Williams & Wilkins, 2002; 1059–98 (Chapter 20).Google Scholar
Bigler, ED. The lesion(s) in traumatic brain injury: Implications for clinical neuropsychology. Arch Clin Neuropsychol 2001; 16: 95–131.CrossRefGoogle ScholarPubMed
Bigler, ED. Structural and functional neuroimaging of traumatic brain injury. In State of the Art Reviews in Physical Medicine and Rehabilitation: Traumatic Brain Injury, McDaeavitt, JT, Ed.. Philadelphia: Hanley and Belfus; 2001: 349–61.Google Scholar
Bigler, ED, Tate, DF. Brain volume, intracranial volume, and dementia. Invest Radiol 2001; 36: 539–46.CrossRefGoogle ScholarPubMed
Blatter, DD, Bigler, ED, Gale, SD, Johnson, SC, Anderson, CV, Burnett, BM, et al. MR-based brain and cerebrospinal fluid measurement after traumatic brain injury: Correlation with neuropsychological outcome. Am J Neuroradiol 1997; 18: 1–10.Google ScholarPubMed
Adams, JH, Graham, DI, Gennarelli, TA, Maxwell, WL. Pathology of non-missile head injury. J Neurol Neurosurg Psychiatry 1991; 54: 481–3.CrossRefGoogle Scholar
Parizel, PM, Ozsarlak, , Goethem, JW, Hauwe, L, Dillen, C, Verlooy, J, et al. Imaging findings in diffuse axonal injury after closed head trauma. Eur Radiol 1998; 8: 960–5.CrossRefGoogle ScholarPubMed
Diaz-Marchan, PJ, Haymam, , Carrier, DA, Feldman, DJ. Computed tomography of closed head injury. In Neurotrauma, Narayan, RK, Wilberger, JE, Povlishock, JT, Eds. New York: McGraw-Hill; 1996: 137–50.Google Scholar
Shibata, Y, Matsumura, A, Meguro, K, Narushima, K.Differentiation of mechanism and prognosis of traumatic brain stem lesions detected by magnetic resonance imaging in the acute stage. Clin Neurol Neurosurg 2000; 102: 124–8.CrossRefGoogle ScholarPubMed
Reichenbach, JR, Venkatesan, R, Schillinger, DJ, Kido, DK, Haacke, EM. Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology 1997; 204: 272–7.CrossRefGoogle ScholarPubMed
Thornhill, S, Teasdale, GM, Murray, GD, McEwen, J, Roy, CW, Penny, KI. Disability in young people and adults one year after head injury: Prospective cohort study. Br Med J 2000: 320: 1631–5.CrossRefGoogle ScholarPubMed
Bigler, ED. Quantitative magnetic resonance imaging in traumatic brain injury. J Head Trauma Rehabil 2001; 16: 117–34.CrossRefGoogle ScholarPubMed
Levin, HS, Williams, DH, Eisenberg, HM, High, WM, Guinto, FC. Serial MRI and neurobehavioural findings after mild to moderate closed head injury. J Neurol Neurosurg Psychiatry 1992; 55: 255–62.CrossRefGoogle ScholarPubMed
Bergsneider, M, Hovda, DA, Shalmon, E, Kelly, DF, Vespa, PM, Martin, NA, et al. Cerebral hyperglycolysis following severe traumatic brain injury in humans: A positron emission tomography study. J Neurosurg 1997; 86: 241–51.CrossRefGoogle ScholarPubMed
Bergsneider, M, Hovda, DA, Lee, SM, Kelly, DF, McArthur, DL, Vespa, PM, et al. Dissociation of cerebral glucose metabolism and level of consciousness during the period of metabolic depression following human traumatic brain injury. J Neurotrauma 2000; 17: 389–401.CrossRefGoogle ScholarPubMed
Glenn, TC, Kelly, DF, Boscardin, WJ, McArthur, DL, Vespa, P, Oertel, M, et al. 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 2003; 23: 1239–50.CrossRefGoogle ScholarPubMed
Hovda, DA, Villablanca, JR, Chugani, HT, Phelps, ME. Cerebral metabolism following neonatal or adult hemineodecortication in cats: I. Effects on glucose metabolism using [14C]2-deoxy-D-glucose autoradiography. J Cereb Blood Flow Metab 1996; 16: 134–46.CrossRefGoogle ScholarPubMed
Hovda, DA, Becker, DP, Katayama, Y. Secondary injury and acidosis. J Neurotrauma 1992; 9(Suppl 1): S47–60.Google ScholarPubMed
Jaggi, JL, Obrist, WD, Gennarelli, TA, Langfitt, TW. Relationship of early cerebral blood flow and metabolism to outcome in acute head injury. J Neurosurg 1990; 72: 176–82.CrossRefGoogle ScholarPubMed
Dusick, JR, Glenn, TC, Lee, WNP, Vespa, PM, Kelly, DF, Lee, SM, et al. Increased pentose phosphate pathway flux after clinical traumatic brain injury: A [1,2–13C2] glucose labeling study in humans. J Cereb Blood Flow Metab 2007; 27: 1593–602.CrossRefGoogle Scholar
Viant, MR, Lyeth, BG, Miller, MG, Berman, RF. An NMR metabolomic investigation of early metabolic disturbances following traumatic brain injury in a mammalian model. NMR Biomed 2005; 18: 507–16.CrossRefGoogle Scholar
Schuhmann, MU, Stiller, D, Skardelly, M, Bernarding, J, Klinge, PM, Samii, A, et al. Metabolic changes in the vicinity of brain contusions: A proton magnetic resonance spectroscopy and histology study. J Neurotrauma 2003; 20: 725–43.CrossRefGoogle ScholarPubMed
Ashwal, S, Holshouser, BA, Shu, SK, Simmons, PL, Perkin, RM, Tomasi, LG, et al. Predictive value of proton magnetic resonance spectroscopy in pediatric closed head injury. Pediatr Neurol 2000; 23: 114–25.CrossRefGoogle ScholarPubMed
Garnett, MR, Blamire, AM, Rajagopalan, B, Styles, P, Cadoux-Hudson, TAD. Evidence for cellular damage in normal-appearing white matter correlates with injury severity in patients following traumatic brain injury: A magnetic resonance spectroscopy study. Brain 2000; 123: 1403–09.CrossRefGoogle ScholarPubMed
Garnett, MR, Blamire, AM, Corkill, RG, Cadoux-Hudson, TAD, Rajagopalan, B, Styles, P. Early proton magnetic resonance spectroscopy in normal-appearing brain correlates with outcome in patients following traumatic brain injury. Brain 2000; 123: 2046–54.CrossRefGoogle ScholarPubMed
Condon, B, Oluoch-Olunya, D, Hadley, D, Teasdale, G, Wagstaff, A. Early 1H magnetic resonance spectroscopy of acute head injury: Four cases. J Neurotrauma 1998; 15: 563–71.CrossRefGoogle ScholarPubMed
Holshouser, BA, Ashwal, S, Luh, GY, Shu, S, Kahlon, S, Auld, KL, et al. 1H-MR spectroscopy after acute CNS injury: Outcome prediction in neonates, infants and children. Radiology 1997; 202: 487–96.CrossRefGoogle Scholar
Holshouser, BA, Ashwal, S, Shu, S, Hinshaw, DB. Proton MR spectroscopy in children with acute brain injury: Comparison of short and long echo time acquisitions. J Magn Reson Imaging 2000; 11: 9–19.3.0.CO;2-6>CrossRefGoogle Scholar
Makoroff, KL, Cecil, KM, Care, M, Bass, WS. Elevated lactate as an early marker of brain injury in inflicted traumatic brain injury. Pediatr Radiol 2005; 35: 668–76.CrossRefGoogle ScholarPubMed
Ashwal, S, Holshouser, B, Tong, K, Serna, T, Osterdock, R, Gross, M, et al. Proton MR spectroscopy detected glutamate/glutamine is increased in children with traumatic brain injury. J Neurotrauma 2004; 21: 1539–52.CrossRefGoogle ScholarPubMed
Baker, AJ, Moulton, RJ, Macmillan, VH, Shedden, PM. Excitatory amino acids in cerebrospinal fluid following traumatic brain injury in humans. J Neurosurg 1993; 79: 369–72.CrossRefGoogle ScholarPubMed
Bullock, R, Zauner, A, Woodward, JJ, Myseros, J, Choi, SC, Ward, JD, et al. Factors affecting excitatory amino acid release following severe human head injury. J Neurosurg 1998; 89: 507–18.CrossRefGoogle ScholarPubMed
Gopinath, SP, Valadka, AB, Goodman, JC, Robertson, CS. Extracellular glutamate and aspartate in head injured patients. Acta Neurochir 2000; 76(suppl): 437–8.Google ScholarPubMed
Ruppel, RA, Clark, RS, Bayir, H, Satchell, MA, Kochanek, PM. Critical mechanisms of secondary damage after inflicted head injury in infants and children. Neurosurg Clin N Am 2002; 13: 169–82.CrossRefGoogle ScholarPubMed
Ashwal, S, Holshouser, B, Tong, K, Serna, T, Osterdock, R, Gross, M, et al. Proton spectroscopy detected myoinisitol in children with Traumatic Brain Injury. Pediatr Res 2004; 56: 630–8.CrossRefGoogle Scholar
Brooks, WM, Stidley, CA, Petropoulos, H, Jung, RE, Weers, DC, Friedman, SD, et al. Metabolic and cognitive response to human traumatic brain injury: A quantitative proton magnetic resonance study. J Neurotrauma 2000; 17: 629–40.CrossRefGoogle ScholarPubMed
Holshouser, BA, Tong, KA, Ashwal, S. Proton MR spectroscopic imaging depicts diffuse axonal injury in children with traumatic brain injury. Am J Neuroradiol 2005; 26: 1276–85.Google ScholarPubMed
Hunter, JV, Thornton, J, Wang, ZJ, Levin, HS, Roberson, G, Brooks, WM, et al. Late proton MR spectroscopy in children after traumatic brain injury: Correlation with cognitive outcomes. Am Neuroradiol 2005; 26: 482–8.Google ScholarPubMed
Flemingham, KL, Baguley, IJ, Green, AM. Effects of diffuse axonal injury on speed of information processing following severe traumatic brain injury. Neuropsychology 2004; 18: 564–71.CrossRefGoogle Scholar
Bibby, H, McDonald, S. Theory of mind after traumatic brain injury. Neuropsychologia 2005; 43: 99–114.CrossRefGoogle ScholarPubMed
Azouvi, P. Neuroimaging correlates of cognitive and functional outcome after traumatic brain injury. Curr Opin Neurol 2000; 13: 665–9.CrossRefGoogle ScholarPubMed
Verger, K, Junque, C, Levin, HS, Jurado, MA, Perez-Gomez, M, Bartres-Faz, D, et al. Correlation of atrophy measures on MRI with neuropsychological sequelae in children and adolescents with traumatic brain injury. Brain Injury 2001; 15: 211–21.Google ScholarPubMed
Yeo, RA, Phillips, JP, Jung, RE, Brown, AJ, Campbell, RC, Brooks, WM. Magnetic resonance spectroscopy detects brain injury and predicts cognitive functioning in children with brain injuries. J Neurotrauma 2006; 23: 1427–35.CrossRefGoogle ScholarPubMed
Ross, BD, Ernst, T, Kreis, R, Hasseler, LJ, Bayer, S, Danielsen, E, et al. 1H MRS in acute traumatic brain injury. J Magn Reson Imaging 1998; 8: 829–40.CrossRefGoogle ScholarPubMed
Nakabayashi, M, Suaki, S, Tomita, MD. Neural injury and recovery near cortical contusions: A clinical magnetic resonance spectroscopy study. J Neurosurg 2007; 106: 270–7.CrossRefGoogle ScholarPubMed
Friedman, SD, Brook, WM, Jung, RE, Hart, BL, Yeo, RA. Proton MR spectroscopic findings correspond to neuropsychological function in traumatic brain injury. Am J Neuroradiol 1998; 19: 1879–85.Google ScholarPubMed
Friedman, SD, Brooks, WM, Jung, RE, Chiulli, SJ, Sloan, JH, Montoya, BT, et al. Quantitative proton MRS predicts outcome after traumatic injury. Neurology 1999; 52: 1384–91.CrossRefGoogle Scholar
Danielsen, ER, Christensen, PB, Arlien-Soborg, P, Thomsen, C. Axonal recovery after severe traumatic brain injury demonstrated in vivo by 1H MR spectroscopy. Neuroradiology 2003; 45: 722–4.CrossRefGoogle ScholarPubMed
Shutter, L, Tong, KA, Holshouser, BA. Proton MRS in acute traumatic brain injury: Role for glutamate/glutamine and choline for outcome prediction. J Neurotrauma 2004; 21: 1693–705.CrossRefGoogle ScholarPubMed
Yoon, SJ, Lee, JH, Kim, ST, Chun, MH. Evaluation of traumatic brain injured patients in correlation with functional status by localized 1H-MR spectroscopy. Clin Rehabil 2005; 19: 209–15.CrossRefGoogle ScholarPubMed
Garnett, MR, Corkill, RG, Blamire, AM, Rajagopalan, B, Manners, DN, Young, JD, et al. Altered cellular metabolism following traumatic brain injury: A magnetic resonance spectroscopy study. J Neurotrauma 2001; 18: 241–6.CrossRefGoogle ScholarPubMed
Zampolini, M, Tarducci, R, Gobbi, G, Franceschini, M, Todeschini, E, Presciutti, O. Localized in vivo 1H-MRS of traumatic brain injury. Eur J Neurol 1997; 4: 246–54.CrossRefGoogle Scholar
Bullock, R, Maxwell, WL, Graham, DI, Teasdale, GM, Adams, JH. Glial swelling following human cerebral contusion: An ultrastructural study. J Neurol Neurosurg Psychiatry 1991; 54: 427–4.CrossRefGoogle Scholar
Liang, D, Bhatta, S, Gerzanich, V, Simard, JM. Cytotoxic edema: Mechanisms of pathological cell swelling. Neurosurg Focus 2007; 22: E2.CrossRefGoogle ScholarPubMed
Simard, JM, Kent, TA, Chen, M, Tarasov, KV, Gerzanich, V. Brain oedema in focal ischaemia: Molecular pathophysiology and theoretical implications. Lancet Neurol 2007; 6: 258–68.CrossRefGoogle ScholarPubMed
Sinson, G, Bagley, LJ, Cecil, KM, Torchia, M, McGowan, JC, Lenkinski, RE, et al. Magnetization transfer imaging and proton MR spectroscopy in the evaluation of axonal injury: Correlation with clinical outcome after traumatic brain injury. Am J Neuroradiol 2001; 22: 143–51.Google ScholarPubMed
Ariza, M, Junque, C, Mataro, M, Paca, MA, Bargallo, N, Olondo, M, et al. Neuropsychological correlates of basal ganglia and medial temporal lobe NAA/Cho reductions in Traumatic Brain Injury. Arch Neurol 2004; 61: 541–4.CrossRefGoogle ScholarPubMed
Uzan, M, Albayram, S. Dashti, SGR, Aydin, S, Hanci, M, Kuday, C. Thalamic proton magnetic resonance spectroscopy in vegetative state induced by traumatic brain injury. J Neurol Neurosurg Psychiatry 2003; 74: 33–8.CrossRefGoogle ScholarPubMed
Jennett, B, Adams, JH, Murray, LS, Graham, DI. Neuropathology in vegetative and severely disabled patients after head injury. Neurology 2001; 56: 486–90.CrossRefGoogle ScholarPubMed
Graham, DI, Maxwell, WL, Adams, JH, Jennett, B. Novel aspects of the neuropathology of the vegetative state after blunt head injury. Prog Brain Res 2005; 150: 445–55.CrossRefGoogle ScholarPubMed
Kirov, I, Fleysher, L, Babb, JS, Silver, JM, Grossman, RI, Gonen, O. Characterizing ‘mild’ in traumatic brain injury with proton MR spectroscopy in the thalamus: Initial findings. Brain Injury 2007; 21: 1147–54.CrossRefGoogle ScholarPubMed
Hillary, FG, Liu, WC, Genova, HM, Maniker, AH, Kepler, K, Greenwald, BD, et al. Examining lactate in severe TBI using proton magnetic resonance spectroscopy. Brain Injury 2007; 21: 981–91.CrossRefGoogle ScholarPubMed
Unterberg, AW, Stover, J, Kress, B, Kiening, KL. Edema and brain trauma. Neuroscience 2004; 129: 1021–9.CrossRefGoogle ScholarPubMed
Vespa, M, McArthur, D, O'Phelan, K, Glenn, T, Etchepare, , Kelly, D, et al. 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 2003; 23: 865–77.CrossRefGoogle ScholarPubMed
Bello, A, Sen, J, Petzold, A, Russo, S, Kitchen, N, Smith, M, et al. Extracellular N-acetylaspartate depletion in traumatic brain injury. J Neurochim 2006; 96: 861–79.CrossRefGoogle Scholar
Signoretti, S, Marmarou, A, Tavazzi, B, Lazzarino, G, Beaumont, A, Vagnozzi, R. N-acetylaspartate reduction as a measure of injury severity and mitochondrial dysfunction following diffuse traumatic brain injury. J Neurotrauma 2001; 18: 977–91.CrossRefGoogle ScholarPubMed
Vagnozzi, R, Tavazzi, B, Stefano, S, Amorini, AM, Belli, A, Cimatti, M, et al. Temporal window of metabolic brain vulnerability to concussions: Mitochondrial-related impairment – Part 1. Neurosurgery 2007; 61: 379–89.CrossRefGoogle Scholar
Tavazzi, B, Vagnozzi, R, Signoretti, S, Amorini, AM, Belli, A, Cimatti, M, et al. Temporal window of metabolic brain vulnerability to concussions: Oxidative and nitrosaive stresses – Part II. Neurosurgery 2007; 61: 390–5.CrossRefGoogle ScholarPubMed
Vagnozzi, R, Signoretti, S, Tavazzi, B, Floris, R, Ludovici, A, Marziali, S, et al. Temporal window of metabolic brain vulnerability to concussion: A pilot 1H-magnetic resonance spectroscopic study in concussed athletes – Part III. Neurosurgery 2008; 62: 1286–96.Google ScholarPubMed
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 Neurochir 2002; 81(suppl): 373–5.Google ScholarPubMed
Macmillan, CSA, Wild, JM, Wardlaw, JM, Andrews, PJD, Marshall, I, Easton, VJ. Traumatic brain injury and subarachnoid hemorrhage: In vivo occult pathology demonstrated by magnetic resonance spectroscopy may not be “ischaemic”. A primary study and review of the literature. Acta Neurochir 2002; 144: 853–62.CrossRefGoogle ScholarPubMed
Holshouser, BA, Tong, KA, Ashwal, S, Oyoyo, U, Ghamsary, M, Saunders, D, et al. Prospective longitudinal proton magnetic resonance spectroscopic imaging in adult traumatic brain injury. J Magn Reson Imaging 2006; 24: 33–40.CrossRefGoogle ScholarPubMed
Shutter, L, Tong, KA, Lee, A, Holshouser, BA. Prognostic role of proton magnetic resonance spectroscopy in acute traumatic brain injury. J Head Trauma Rehabil 2006; 21: 334–49.CrossRefGoogle ScholarPubMed
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. J Neurol Neurosurg Psychiatry 2007; 78: 501–07.CrossRefGoogle ScholarPubMed
Signoretti, S, Marmarou, A, Aygok, GA, Fatouros, PP, Portella, G, Bullock, RM. Assessment of mitochondrial impairment in traumatic brain injury using high-resolution proton magnetic resonance spectroscopy. J Neurosurg 2008; 108: 42–52.CrossRefGoogle ScholarPubMed
Govindaraju, V, Gauger, GE, Manley, GT, Andreas, E, Meeker, M, Maudsley, AA. Volumetric proton spectroscopic imaging of mild traumatic brain injury. Am J Neuroradiol 2004; 25: 730–7.Google ScholarPubMed
Cohen, BA, Inglese, M, Rusinek, H, Babb, JS, Grossman, RO, Gonen, O. Proton MR spectroscopy and MRI-volumetry in mild traumatic brain injury. Am J Neuroradiol 2007; 28: 907–13.Google ScholarPubMed
Babikian, T, Freier, MC, Tong, KA, Nickerson, JP, Wall, CJ, Holshouser, BA, et al. Susceptibility-weighted imaging: Neuropsychological outcome and pediatric head injury. Pediatr Neurol 2005; 33: 179–89.CrossRefGoogle ScholarPubMed
Ashwal, S, Babikian, T, Gardner-Nichols, J, Freier, M-C, Tong, KA, Holshouser, BA. Susceptibility-weighted imaging and proton magnetic resonance spectroscopy in assessment of outcome after pediatric traumatic brain injury. Arch Phys Med Rehabil 2008; 82: S50–7.Google Scholar
Beaumont, A, Fatouros, P, Gennarelli, T, Corwin, F, Marmarou, A. Bolus tracer delivery measured by MRI confirms edema without blood–brain barrier permeability in diffuse traumatic brain injury. Acta Neurochir 2006; 96(suppl): 171–4.CrossRefGoogle ScholarPubMed
Hendrich, KS, Kochanek, PM, Williams, DS, Schiding, JK, Marion, DW, Ho, C. Early perfusion after controlled cortical impact in rats: Quantification by arterial spin-labeled MRI and the influence of spin-lattice relaxation time heterogeneity. Magn Reson Med 1999; 42: 673–81.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Rousseau, MC, Confort-Gouny, S, Catala, A, Graperon, J, Blaya, J, Soulier, E, et al. A MRS-MRI-fMRI exploration of the brain. Impact of long-lasting persistent vegetative state. Brain Injury 2008; 22: 123–34.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats