Assessment of metabolic brain damage and recovery following mild traumatic brain injury: A multicentre, proton magnetic resonance spectroscopic study in concussed patients

Brain

Volumn 133, Issue 11, 2010, Pages 3232-3242

  Vagnozzi, Roberto ^a   Signoretti, Stefano ^b   Cristofori, Luciano ^c   Alessandrini, Franco ^c   Floris, Roberto ^a   Isgró, Eugenio ^d   Ria, Antonio ^c   Marziale, Simone ^a   Zoccatelli, Giada ^c   Tavazzi, Barbara ^e   Del Bolgia, Franco ^a   Sorge, Roberto ^a   Broglio, Steven P ^f   McIntosh, Tracy K ^g   Lazzarino, Giuseppe ^h  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b SAN CAMILLO FORLANINI HOSPITAL   (Italy)

^c MAGGIORE HOSPITAL   (Italy)

^d UNIVERSITY OF PARMA   (Italy)

^e CATHOLIC UNIVERSITY   (Italy)

^f UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^g Media NeuroConsultants Inc   (United States)

^h UNIVERSITY OF CATANIA   (Italy)

Author keywords

metabolic brain vulnerability; mild traumatic brain injury; N acetylaspartate; sport related concussion

Indexed keywords

CHOLINE DERIVATIVE; CREATINE; N ACETYLASPARTIC ACID;

ACCURACY; ADOLESCENT; ADULT; ARTICLE; ATHLETE; BRAIN CONCUSSION; BRAIN DAMAGE; BRAIN METABOLISM; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CLINICAL FEATURE; CLINICAL TRIAL; COMPARATIVE STUDY; CONTROL GROUP; CONTROLLED STUDY; FEMALE; HOSPITAL ADMISSION; HUMAN; MAGNETIC FIELD; MALE; MULTICENTER STUDY; NON INVASIVE PROCEDURE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTON NUCLEAR MAGNETIC RESONANCE; SPORT INJURY; TRAUMATIC BRAIN INJURY;

EID: 78049484731     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awq200     Document Type: Article

References (66)

1. Andersen BJ, Marmarou A. Post-traumatic selective stimulation of glycolysis. Brain Res 1992; 585: 184-9.
2. Barth JT, Freeman JR, Broshek DK, Varney RN. Acceleration-deceleration sport-related concussion: the gravity of it all. J Athl Train 2001; 36: 253-6.
3. Baslow MH. Brain N-acetylaspartate as a molecular water pump and its role in the etiology of Canavan disease: A mechanistic explanation. J Mol Neurosci 2003a; 21: 185-90.
4. Baslow MH. N-acetylaspartate in the vertebrate brain: metabolism and function. Neurochem Res 2003b; 28: 941-53.
5. Benedetti B, Rigotti DJ, Liu S, Filippi M, Grossman RI, Gonen O. Reproducibility of the whole-brain N-acetylaspartate level across institutions, MR scanners, and field strengths. AJNR Am J Neuroradiol 2007; 28: 72-5.
6. 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.
7. Broglio SP, Macciocchi SN, Ferrara MS. Sensitivity of the concussion assessment battery. Neurosurgery 2007; 60: 1050-8.
8. Cantu RC. Recurrent athletic head injury: risks and when to retire. Clin Sports Med 2003; 22: 593-603.
9. Cantu RC. Athletic concussion: current understanding as of 2007. Neurosurgery 2007; 60: 963-4.
10. Cohen BA, Inglese M, Rusinek H, Babb JS, Grossman RI, Gonen O. Proton MR spectroscopy and MRI-volumetry in mild traumatic brain injury. AJNR Am J Neuroradiol 2007; 28: 907-13.
11. Davis GA, Iverson GL, Guskiewicz KM, Ptito A, Johnston KM. Contributions of neuroimaging, balance testing, electrophysiology and blood markers to the assessment of sport-related concussion. Br J Sports Med 2009; 43 (Suppl 1): i36-45.
12. Delaney JS, Abuzeyad F, Correa JA, Foxford R. Recognition and characteristics of concussions in the emergency department population. J Emerg Med 2005; 29: 189-97.
13. Engberg AW, Teasdale TW. Traumatic brain injury in Denmark 1979-1996: A national study of incidence and mortality. Eur J Epidemiol 2001; 17: 437-42.
14. Foda MA, Marmarou A. A new model of diffuse brain injury in rats: part II. Morphological characterization. J Neurosurg 1994; 80: 301-13.
15. 1H-magnetic resonance spectroscopy study. J Neurotrauma 2009; 26: 1635-43.
16. Gerberding JL. for the National Center for Injury Prevention and Control. Report to congress on mild traumatic brain injury in the United States\-steps to prevent a serious public health problem. Atlanta Centers for Disease Control and Prevention 2003. 31-7.
17. Giza CC, Hovda DA. The neurometabolic cascade of concussion. J Athl Train 2001; 36: 228-35.
18. Gosselin N, Lassonde M, Petit D, Leclerc S, Mongrain V, Collie A, et al. Sleep following sport-related concussions. Sleep Med 2009; 10: 35-46.
19. Guskiewicz KM, McCrea M, Marshall SW, Cantu RC, Randolph C, Barr W, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003; 290: 2549-55.
20. Guskiewicz KM, Bruce SL, Cantu RC, Ferrara MS, Kelly JP, McCrea M, et al. National Athletic Trainers' Association: Research based recommendations on management of sport related concussion: summary of the National Athletic Trainers' Association position statement. Br J Sports Med 2006; 40: 6-10.
21. Henry LC, Tremblay S, Boulanger Y, Ellemberg D, Lassonde M. Neurometabolic changes in the acute phase after sports concussions correlate with symptom severity. J Neurotrauma 2010; 27: 65-76.
22. Hovda DA, Badie H, Karimi S, Thomas S, Yoshino A, Kawamata T, et al. Concussive brain injury produces a state of vulnerability for intracranial pressure perturbation in the absence of morphological damage. In: Avezaat CJ, van Eijndhoven JH, Maas AI, Tans JT, editors. Intracranial pressure VIII. New York: Springer; 1993. p. 469-72.
23. Hovda DA, Prins M, Becker DP, Lee S, Bergsneider M, Martin NA. Neurobiology of concussion. In: Bailes JE, Lovell MR, Maroon JC, editors. Sports related concussion. St Louis, MO: Quality Medical Publishing, Inc.; 1999. p. 12-51.
24. Hunt T, Asplund C. Concussion assessment and management. Clin Sports Med 2010; 29: 5-17.
25. Jenkins LW, Marmarou A, Lewelt W, Becker DP. Increased vulnerability of the traumatized brain to early ischemia. In: Baethmann A, Go KG, Unterberg A, editors. Mechanisms of secondary brain injury. New York: Plenum; 1986. p. 273-82.
26. Jenkins LW, Moszynski K, Lyeth BG, Lewelt W, DeWitt DS, Allen A, et al. Increased vulnerability of the mildly traumatized rat brain to cerebral ischemia: the use of controlled secondary ischemia as a research tool to identify common or different mechanisms contributing to mechanical and ischemic brain injury. Brain Res 1989; 477: 211-24.
27. Kissick J, Johnstone KM. Return to play after concussion: principles and practice. Clin J Sport Med 2005; 15: 426-31.
28. Kurca E, Sivák S, Kucera P. Impaired cognitive functions in mild traumatic brain injury patients with normal and pathologic magnetic resonance imaging. Neuroradiology 2006; 48: 661-9.
29. Lifshitz J, Friberg H, Neumar RW, Raghupathi R, Welsh FA, Janmey P, et al. Structural and functional damage sustained by mitochondria after traumatic brain injury in the rat: evidence for differentially sensitive populations in the cortex and hippocampus. J Cereb Blood Flow Metab 2003; 23: 219-31.
30. Longhi L, Saatman KE, Fujimoto S, Raghupathi R, Meaney DF, Davis J, et al. Temporal window of vulnerability to repetitive experimental concussive brain injury. Neurosurgery 2005; 56: 364-74.
31. Lovell M, Collins M, Bradley J. Return to play following sports-related concussion. Clin Sports Med 2004; 23: 421-41.
32. Madhavarao CN, Chinopoulos C, Chandrasekaran K, Namboodiri MA. Characterization of the N-acetylaspartate biosynthetic enzyme from rat brain. J Neurochem 2003; 86: 824-35.
33. Madhavarao CN, Moffett JR, Moore RA, Viola RE, Namboodiri MA, Jacobowitz DM. Immunohistochemical localization of aspartoacylase in the rat central nervous system. J Comp Neurol 2004; 472: 318-29.
34. Marmarou A, Foda MA, van den Brink W, Campbell J, Kita H, Demetriadou K. A new model of diffuse brain injury in rats: part I. Pathophysiology and biomechanics. J Neurosurg 1994; 80: 291-300.
35. McClincy MP, Lovell MR, Pardini J, Collins MW, Spore MK. Recovery from sports concussion in high school and collegiate athletes. Brain Inj 2006; 20: 33-9.
36. McCrea M, Guskiewicz KM, Marshall SW, Barr W, Randolph C, Cantu RC, et al. Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003; 290: 2556-63.
37. McCrea M, Hammeke T, Olsen G, Leo P, Guskiewicz K. Unreported concussion in high school football players: implications for prevention. Clin J Sport Med 2004; 14: 13-7.
38. McCrory P, Meeuwisse W, Johnston K, Dvorak J, Aubry M, Molloy M, et al. Consensus statement on concussion in sport: the 3rd International Conference on Concussion in Sport held in Zurich, November 2008. Br J Sports Med 2009a; 43 (Suppl 1): i76-90.
39. McCrory P, Meeuwisse W, Johnston K, Dvorak J, Aubry M, Molloy M, et al. Consensus statement on concussion in sport: the 3rd International Conference on Concussion in Sport held in Zurich, November 2008. J Clin Neurosci 2009b; 16: 755-63.
40. Meehan WP 3rd, Bachur RG. Sport-related concussion. Pediatrics 2009; 123: 114-23.
41. Mehta V, Namboodiri MA. N-acetylaspartate as an acetyl source in the nervous system. Brain Res Mol Brain Res 1995; 31: 151-7.
42. Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AM. N-Acetylaspartate in the CNS: from neurodiagnostics to neurobiology. Prog Neurobiol 2007; 81: 89-131.
43. Moreno A, Ross BD, Bluml S. Direct determination of the N-acetyl-L-aspartate synthesis rate in the human brain by (13)C MRS and [1-(13)C]glucose infusion. J Neurochem 2001; 77: 347-50.
44. Nakabayashi M, Suzaki S, Tomita H. Neural injury and recovery near cortical contusions: A clinical magnetic resonance spectroscopy study. J Neurosurg 2007; 106: 370-7.
45. Pellman EJ, Viano DC, Casson IR, Tucker AM, Waeckerle JF, Powell JW, et al. Concussion in professional football. Repeat injuries\-Part 4. Neurosurgery 2004; 55: 860-76.
46. Ponsford J. Rehabilitation interventions after mild head injury. Curr Opin Neurol 2005; 18: 692-7.
47. Praticò D, Reiss P, Tang LX, Sung S, Rokach J, McIntosh TK. Local and systemic increase in lipid peroxidation after moderate experimental traumatic brain injury. J Neurochem 2002; 80: 894-8.
48. Randolph C, Millis S, Barr WB, McCrea M, Guskiewicz KM, Hammeke TA, et al. Concussion symptom inventory: an empirically derived scale for monitoring resolution of symptoms following sport-related concussion. Arch Clin Neuropsychol 2009; 24: 219-29.
49. Register-Mihalik JK, Mihalik JP, Guskiewicz KM. Balance deficits after sports-related concussion in individuals reporting posttraumatic headache. Neurosurgery 2008; 63: 76-80.
50. Rigotti DJ, Inglese M, Gonen O. Whole-brain N-acetylaspartate as a surrogate marker of neuronal damage in diffuse neurologic disorders. AJNR Am J Neuroradiol 2007; 28: 1843-9.
51. Robertson CL, Soane L, Siegel ZT, Fiskum G. The potential role of mitochondria in pediatric traumatic brain injury. Dev Neurosci 2006; 28: 432-46.
52. Sarmento E, Moreira P, Brito C, Souza J, Jevoux C, Bigal M. Proton spectroscopy in patients with post-traumatic headache attributed to mild head injury. Headache 2009; 49: 1345-52.
53. Saunders RL, Harbaugh RE. The second impact in catastrophic contact-sports head trauma. JAMA 1984 252 538-9.
54. Schatz P, Pardini JE, Lovell MR, Collins MW, Podell K. Sensitivity and specificity of the ImPACT Test Battery for concussion in athletes. Arch Clin Neuropsychol 2006; 21: 91-9.
55. Schleimer JA. Minor traumatic brain injury in sports. Curr Sports Med Rep 2002; 1: 323-6.
56. 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.
57. 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 spectros-copy. J Neurosurg 2008; 108: 42-52.
58. Signoretti S, Di Pietro V, Vagnozzi R, Lazzarino G, Amorini AM, Belli A, et al. Transient alterations of creatine, creatine phosphate, N-acetylas-partate and high-energy phosphates after mild traumatic brain injury in the rat. Mol Cell Biochem 2010; 333: 269-77.
59. 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. AJNR Am J Neuroradiol 2001; 22: 143-51.
60. Tagliaferri F, Compagnone C, Korsic M, Servadei F, Kraus J. A systematic review of brain injury epidemiology in Europe. Acta Neurochirurgica 2006; 148: 255-68.
61. Tavazzi B, Signoretti S, Lazzarino G, Amorini AM, Delfini R, Cimatti M, et al. Cerebral oxidative stress and depression of energy metabolism correlate with severity of diffuse brain injury in rats. Neurosurgery 2005; 56: 582-9.
62. Tavazzi B, Vagnozzi R, Signoretti S, Amorini AM, Belli A, Cimatti M, et al. Temporal window of metabolic brain vulnerability to concussions: oxidative and nitrosative stresses-part II. Neurosurgery 2007; 61: 390-6.
63. Vagnozzi R, Marmarou A, Tavazzi B, Signoretti S, Di Pierro D, Del Bolgia F, et al. Changes of cerebral energy metabolism and lipid per-oxidation in rats leading to mitochondrial dysfunction after diffuse brain injury. J Neurotrauma 1999; 16: 903-13.
64. Vagnozzi R, Signoretti S, Tavazzi B, Cimatti M, Amorini AM, Donzelli S, et al. Hypothesis of the postconcussive vulnerable brain: experimental evidence of its metabolic occurrence. Neurosurgery 2005; 57: 164-71.
65. Vagnozzi R, Tavazzi B, Signoretti S, Amorini AM, Belli A, Cimatti M, et al. Temporal window of metabolic brain vulnerability to concussions: mitochondrial-related metabolic impairment-part I. Neurosurgery 2007; 61: 379-89.
66. 1H-magnetic resonance spectroscopic study in concussed athletes\-part III. Neurosurgery 2008; 62: 1286-95.