Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2022, 166(1):84-90 | DOI: 10.5507/bp.2021.029

Proton magnetic resonance spectroscopy changes in the brainstem in patients after mild traumatic brain injury with loss of consciousness

Robert Ruzinaka, Michal Bittsanskyb, Martina Martinikovac, Vladimir Nosala, Ema Kantorovaa, Jana Ballovaa, Monika Turcanova Koprusakovaa, Petra Hnilicovab, Marian Grendarb, Robert Dusenkad, Branislav Kolarovszkie, Kamil Zelenakf, Egon Kurcaa, Stefan Sivaka
a Clinic of Neurology, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Slovak Republic
b Biomedical Center Martin, Jessenius Faculty of Medicine in Martin, Comenius University in Bratilava, Slovak Republic
c Department of Neurology, F.D. Roosevelt Hospital, Banská Bystrica, Slovak Republic
e Clinic of Neurosurgery, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Slovak Republic
f Clinic of Radiology, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Slovak Republic

Introduction: Loss of consciousness (LOC) is used as a diagnostic feature of mild traumatic brain injury (MTBI). However, only 10% of concussions result in LOC. There are only a limited number of in-vivo studies dealing with unconsciousness and structural and functional integrity of the brainstem in patients with MTBI. The aim of our pilot study was to assess the sensitivity of proton magnetic resonance spectroscopy (1H-MRS) to detect metabolic changes in the brainstem in patients after MTBI with unconscioussness.

Methods: Twenty-four patients (12 with LOC, and 12 without LOC) within 3 days of MTBI and 19 healthy controls were examined. All subjects underwent single-voxel 1H-MRS examination of the upper brainstem. Spectra were evaluated using LCModel software. Ratios of total N-acetylaspartate (tNAA), total choline-containing compounds (tCho) and glutamate plus glutamine (Glx) to total creatine (tCre) were used for calculations.

Results: We found a significant decrease in tNAA/tCre and tCho/tCre ratios in the patient group with LOC when compared with the control group of healthy volunteers (P=0.002 and P=0.041, respectively), and a significant decrease in the tNAA/tCre ratio in the LOC group when compared with patients without LOC (P=0.04). Other metabolite ratios in the brainstem did not show any significant group differences.

Conclusion: Our findings indicate that decrease of tNAA/tCre ratio in the upper brainstem using single-voxel 1H-MRS may provide a potential biomarker for MTBI associated with LOC.

Keywords: mild traumatic brain injury, concussion, loss of consciousness, magnetic resonance spectroscopy

Received: November 18, 2020; Revised: April 20, 2021; Accepted: April 26, 2021; Prepublished online: May 11, 2021; Published: March 1, 2022  Show citation

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Ruzinak, R., Bittsansky, M., Martinikova, M., Nosal, V., Kantorova, E., Ballova, J., ... Sivak, S. (2022). Proton magnetic resonance spectroscopy changes in the brainstem in patients after mild traumatic brain injury with loss of consciousness. Biomedical papers166(1), 84-90. doi: 10.5507/bp.2021.029
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References

  1. Carroll LJ, Cassidy JD, Holm L, Kraus J, Coronado VG; WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. Methodological issues and research recommendations for mild traumatic brain injury: the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. J Rehabil Med 2004;(43 Suppl):113-25. Go to original source... Go to PubMed...
  2. McCrory P, Meeuwisse WH, Aubry M, Cantu RC, Dvořák J, Echemendia RJ, Engebretsen L, Johnston K, Kutcher JS, Raftery M, Sills A, Benson BW, Davis GA, Ellenbogen R, Guskiewicz KM, Herring SA, Iverson GL, Jordan BD, Kissick J, McCrea M, McIntosh AS, Maddocks D, Makdissi M, Purcell L, Putukian M, Schneider K, Tator CH, Turner M. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport, Zurich, November 2012. J Athl Train 2013;48(4):554-75.
  3. Edlow BL, Giacino JT, Wu O. Functional MRI and outcome in traumatic coma. Curr Neurol Neurosci Rep 2013;13(9):375. Go to original source... Go to PubMed...
  4. Snider SB, Bodien YG, Bianciardi M, Brown EN, Wu O, Edlow BL. Disruption of the ascending arousal network in acute traumatic disorders of consciousness. Neurology 2019;93(13):e1281-e87. Go to original source... Go to PubMed...
  5. Moruzzi G, Magoun HW. Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1949;1(4):455-73. Go to original source...
  6. Plum F, Posner JB. States of acutely altered consciousness. In: Plum F, Posner JB, editors. The Diagnosis of Stupor and Coma. 3rd ed. Philadelphia, PA: FA Davis; 1982. p. 3-5.
  7. Mitchell DE, Adams JH. Primary focal impact damage to the brainstem in blunt head injuries. Does it exist? Lancet 1973;2(7823):215-18. Go to original source... Go to PubMed...
  8. Smith DH, Nonaka M, Miller R, Leoni M, Chen XH, Alsop D, Meaney DF. Immediate coma following inertial brain injury dependent on axonal damage in the brainstem. J Neurosurg 2000;93(2):315-22. Go to original source... Go to PubMed...
  9. Ommaya AK, Gennarelli TA. Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries. Brain 1974;97(4):633-54. Go to original source... Go to PubMed...
  10. Brown WJ, Yoshida N, Canty T, Verity MA. Experimental concussion. Ultrastructural and biochemical correlates. Am J Pathol 1972;67:41-68.
  11. Jane JA, Steward O, Gennarelli T. Axonal degeneration induced by experimental noninvasive minor head injury. J Neurosurg 1985;62:96-100. Go to original source... Go to PubMed...
  12. Browne KD, Chen XH, Meaney DF, Smith DH. Mild traumatic brain injury and diffuse axonal injury in swine. J Neurotrauma 2011;28(9):1747-55. Go to original source... Go to PubMed...
  13. Einarsen CE, Moen KG, Håberg AK, Eikenes L, Kvistad KA, Xu J, Moe HK, Tollefsen MH, Vik A, Skandsen T. Patients with Mild Traumatic Brain Injury Recruited from Both Hospital and Primary Care Settings: A Controlled Longitudinal Magnetic Resonance Imaging Study. J Neurotrauma 2019;36(22):3172-182. Go to original source... Go to PubMed...
  14. Firsching R, Woischneck D, Diedrich M, Klein S, Ruckert A, Wittig H, Dohring W. Early magnetic resonance imaging of brainstem lesions after severe head injury. J Neurosurg 1998;89:707-12. Go to original source... Go to PubMed...
  15. Weiss N, Galanaud D, Carpentier A, Tezenas de Montcel S, Naccache L, Coriat P, Puybasset L. A combined clinical and MRI approach for outcome assessment of traumatic head injured comatose patients. J Neurol 2008;255(2):217-23. Go to original source... Go to PubMed...
  16. Carpentier A, Galanaud D, Puybasset L, Muller JC, Lescot T, Boch AL, Riedl V, Cornu P, Coriat P, Dormont D, van Effenterre R. Early morphologic and spectroscopic magnetic resonance in severe traumatic brain injuries can detect "invisible brain stem damage" and predict "vegetative states". J Neurotrauma 2006;23(5):674-85. Go to original source... Go to PubMed...
  17. Jang SH, Kwon HG. Injury of the Ascending Reticular Activating System in Patients With Fatigue and Hypersomnia Following Mild Traumatic Brain Injury: Two Case Reports. Medicine (Baltimore) 2016;95(6):e2628. Go to original source... Go to PubMed...
  18. Delano-Wood L, Bangen KJ, Sorg SF, Clark AL, Schiehser DM, Luc N, Bondi MW, Werhane M, Kim RT, Bigler ED. Brainstem white matter integrity is related to loss of consciousness and postconcussive symptomatology in veterans with chronic mild to moderate traumatic brain injury. Brain Imaging Behav 2015;9(3):500-12. Go to original source... Go to PubMed...
  19. Matthews SC, Spadoni AD, Lohr JB, Strigo IA, Simmons AN. Diffusion tensor imaging evidence of white matter disruption associated with loss versus alteration of consciousness in warfighters exposed to combat in Operations Enduring and Iraqi Freedom. Psychiatry Res 2012;204(2-3):149-54. Go to original source... Go to PubMed...
  20. Gonzalez PG, Walker MT. Imaging modalities in mild traumatic brain injury and sports concussion. PM&R 2011;3(10 Suppl 2): S413-24. Go to original source... Go to PubMed...
  21. Sivák Š, Bittšanský M, Grossmann J, Nosál' V, Kantorová E, Siváková J, Demková A, Hnilicová P, Dobrota D, Kurča E. Clinical correlations of proton magnetic resonance spectroscopy findings in acute phase after mild traumatic brain injury. Brain Inj 2014;28(3):341-6. Go to original source... Go to PubMed...
  22. Provencher SW. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 2001;14(4):260-4. Go to original source... Go to PubMed...
  23. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing 2020, Vienna, Austria. URL https://www.R-project.org/.
  24. 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(5):907-13.
  25. Cartwright PE, Perkins TG, Wilson SH, Weaver LK, Orrison WW. Analysis of magnetic resonance spectroscopy relative metabolite ratios in mild traumatic brain injury and normative controls. Undersea Hyperb Med 2019;46(3):291-97. Go to original source...
  26. 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 Inj 2007;21(11):1147-54. Go to original source... Go to PubMed...
  27. Signoretti S, Vagnozzi R, Tavazzi B, Lazzarino G. Biochemical and neurochemical sequelae following mild traumatic brain injury: summary of experimental data and clinical implications. Neurosurg Focus 2010;29(5):E1. Go to original source... Go to PubMed...
  28. Govind V, Gold S, Kaliannan K, Saigal G, Falcone S, Arheart KL, Harris L, Jagid J, Maudsley AA. Whole-brain proton MR spectroscopic imaging of mild-to-moderate traumatic brain injury and correlation with neuropsychological deficits. J Neurotrauma 2010;27(3):483-96. Go to original source... Go to PubMed...
  29. Veeramuthu V, Seow P, Narayanan V, Wong JHD, Tan LK, Hernowo AT, Ramli N. Neurometabolites Alteration in the Acute Phase of Mild Traumatic Brain Injury (mTBI): An In Vivo Proton Magnetic Resonance Spectroscopy (1H-MRS) Study. Acad Radiol 2018;25(9):1167-77. Go to original source... Go to PubMed...
  30. Stovell MG, Yan JL, Sleigh A, Mada MO, Carpenter TA, Hutchinson PJA, Carpenter KLH. Assessing Metabolism and Injury in Acute Human Traumatic Brain Injury with Magnetic Resonance Spectroscopy: Current and Future Applications. Front Neurol 2017;8:426. Go to original source... Go to PubMed...

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