CC BY-NC-ND 4.0 · Arq Neuropsiquiatr 2018; 76(03): 189-199
DOI: 10.1590/0004-282X20180007
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Current contribution of diffusion tensor imaging in the evaluation of diffuse axonal injury

Contribuição atual da imagem por tensor de difusão na avaliação da lesão axonal difusa
Daphine Centola Grassi
1   Universidade de São Paulo, Faculdade de Medicina, Departamento de Radiologia, São Paulo SP, Brasil.
,
David Macedo da Conceição
1   Universidade de São Paulo, Faculdade de Medicina, Departamento de Radiologia, São Paulo SP, Brasil.
,
Claudia da Costa Leite
1   Universidade de São Paulo, Faculdade de Medicina, Departamento de Radiologia, São Paulo SP, Brasil.
,
Celi Santos Andrade
1   Universidade de São Paulo, Faculdade de Medicina, Departamento de Radiologia, São Paulo SP, Brasil.
› Author Affiliations

ABSTRACT

Traumatic brain injury (TBI) is the number one cause of death and morbidity among young adults. Moreover, survivors are frequently left with functional disabilities during the most productive years of their lives. One main aspect of TBI pathology is diffuse axonal injury, which is increasingly recognized due to its presence in 40% to 50% of all cases that require hospital admission. Diffuse axonal injury is defined as widespread axonal damage and is characterized by complete axotomy and secondary reactions due to overall axonopathy. These changes can be seen in neuroimaging studies as hemorrhagic focal areas and diffuse edema. However, the diffuse axonal injury findings are frequently under-recognized in conventional neuroimaging studies. In such scenarios, diffuse tensor imaging (DTI) plays an important role because it provides further information on white matter integrity that is not obtained with standard magnetic resonance imaging sequences. Extensive reviews concerning the physics of DTI and its use in the context of TBI patients have been published, but these issues are still hazy for many allied-health professionals. Herein, we aim to review the current contribution of diverse state-of-the-art DTI analytical methods to the understanding of diffuse axonal injury pathophysiology and prognosis, to serve as a quick reference for those interested in planning new studies and who are involved in the care of TBI victims. For this purpose, a comprehensive search in Pubmed was performed using the following keywords: “traumatic brain injury”, “diffuse axonal injury”, and “diffusion tensor imaging”.

RESUMO

O traumatismo cranioencefálico (TCE) é a principal causa de morbimortalidade entre adultos jovens. Aqueles que sobrevivem são frequentemente deixados com sequelas funcionais nos anos mais produtivos de suas vidas. O principal aspecto fisiopatológico do TCE é a lesão axonial difusa (LAD), cada vez mais destacada pois está presente em 40 a 50% dos casos que necessitam de internação hospitalar. LAD é definida como a injúria axonial extensa caracterizada pela axoniotomia completa assim como pelas reações secundárias a axoniopatia, que são demonstradas por métodos de neuroimagem como áreas de edema e micro-hemorragia. Entretanto, os achados da LAD são frequentemente subestimados em estudos de neuroimagem convencional. É neste contexto que imagens por tensor de difusão (DTI) ganharam ênfase, já que permitem obter informações sobre a integridade da substância branca que não eram obtidas por sequências convencionais de ressonância magnética (RM). Existem artigos extensos sobre os fundamentos físicos e as aplicações de DTI em pacientes vítimas de TCE, no entanto, estes assuntos permanecem ainda nebulosos a alguns profissionais da área de saúde. Deste modo, propomos uma revisão didática sobre a contribuição do estado da arte de diferentes métodos analíticos de DTI no entendimento do processo da fisiopatologia e prognóstico da LAD, servindo assim como uma ferramenta acessível para aqueles interessados em planejamento de novos estudos e aqueles envolvidos no tratamento de vítimas de TCE. Uma pesquisa abrangente foi realizada no Pubmed com as seguintes palavras-chave: “traumatismo cranioencefálico”, “lesão axonial difusa”, “imagem por tensor de difusão”.

Support

Grants 2015/18136-1, 2016/05547-6 and 2017/17065-9 from São Paulo Research Foundation – FAPESP.




Publication History

Received: 17 October 2017

Accepted: 12 December 2017

Article published online:
28 August 2023

© 2023. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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  • References

  • 1 Corso P Finkelstein E, Miller T, Fiebelkorn I, Zaloshnja E. Incidence and lifetime costs of injuries in the United States. Inj Prev. 2006;12(4):212-8. https://doi.org/10.1136/ip.2005.010983
  • 2 Greve MW, Zink BJ. Pathophysiology of traumatic brain injury. Mt Sinai J Med. 2009;76(2):97-104. https://doi.org/10.1002/msj.20104
  • 3 Morais DF, Spotti AR, Tognola WA, Gaia FF, Andrade AF. Clinical application of magnetic resonance in acute traumatic brain injury. Arq Neuropsiquiatr. 2008 Mar;66(1):53-8. https://doi.org/10.1590/S0004-282X2008000100013
  • 4 Andrade AF, Paiva WS, Amorim RL, Figueiredo EG, Rusafa Neto E, Teixeira MJ. [The pathophysiological mechanisms following traumatic brain injury]. Rev Assoc Med Bras (1992). 2009 Jan-Feb;55(1):75-81. Portuguese. https://doi.org/10.1590/S0104-42302009000100020
  • 5 Sandsmark DK. Clinical outcomes after traumatic brain injury. Curr Neurol Neurosci Rep. 2016;16(6):52. https://doi.org/10.1007/s11910-016-0654-5.
  • 6 Vieira RC, Paiva WS, Oliveira DV, Teixeira MJ, Andrade AF, Sousa RM. Diffuse axonal injury: epidemiology, outcome and associated risk factors. Front Neurol. 2016 Oct;7:178. https://doi.org/10.3389/fneur.2016.00178
  • 7 Provenzale JM. Imaging of traumatic brain injury: a review of the recent medical literature. AJR Am J Roentgenol. 2010;194(1):16-19. https://doi.org/10.2214/AJR.09.3687
  • 8 Skandsen T, Kvistad KA, Solheim O, Strand IH, Folvik M, Vik A. Prevalence and impact of diffuse axonal injury in patients with moderate and severe head injury: a cohort study of early magnetic resonance imaging findings and 1-year outcome. J Neurosurg. 2010;113(3):556-563. https://doi.org/10.3171/2009.9.JNS09626
  • 9 Li J, Li XY, Feng DF, Pan DC. Biomarkers associated with diffuse traumatic axonal injury: exploring pathogenesis, early diagnosis, and prognosis. J Trauma. 2010 Dec;69(6):1610-8. https://doi.org/10.1097/TA.0b013e3181f5a9ed
  • 10 Olsson A, Csajbok L, Ost M, Höglund K, Nylén K, Rosengren L et al. Marked increase of beta-amyloid(1-42) and amyloid precursor protein in ventricular cerebrospinal fluid after severe traumatic brain injury. J Neurol. 2004 Jul;251(7):870-6. https://doi.org/10.1007/s00415-004-0451-y
  • 11 Magnoni S, Esparza TJ, Conte V, Carbonara M, Carrabba G, Holtzman DM et al. Tau elevations in the brain extracellular space correlate with reduced amyloid-β levels and predict adverse clinical outcomes after severe traumatic brain injury. Brain. 2012 Apr;135(Pt 4):1268-80. https://doi.org/10.1093/brain/awr286
  • 12 Büki A, Povlishock JT. All roads lead to disconnection? Traumatic axonal injury revisited. Acta Neurochir (Wien). 2006 Feb;148(2):181-93. https://doi.org/10.1007/s00701-005-0674-4
  • 13 Chen YJ, Nabavizadeh SA, Vossough A, Kumar S, Loevner LA, Mohan S. Wallerian degeneration beyond the corticospinal tracts: conventional and advanced MRI findings. J Neuroimaging. 2017 May;27(3):272-80. https://doi.org/10.1111/jon.12404
  • 14 Meythaler JM, Peduzzi JD, Eleftheriou E, Novack TA. Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch Phys Med Rehabil. 2001;82(10):1461-1471. https://doi.org/10.1053/apmr.2001.25137
  • 15 Magnoni S, Brody DL. New perspectives on amyloid-beta dynamics after acute brain injury moving between experimental approaches and studies in the human brain. Arch Neurol. 2010;67(9):1068-1073. https://doi.org/10.1001/archneurol.2010.214
  • 16 Adams JH, Doyle D, Ford I, Gennarelli TA, Graham DI, McLellan DR. Diffuse axonal injury in head-injury - definition, diagnosis and grading. Histopathology. 1989;15(1):49-59. https://doi.org/10.1111/j.1365-2559.1989.tb03040.x
  • 17 Shenton ME, Hamoda HM, Schneiderman JS, Bouix S, Pasternak O, Rathi Y et al. A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav. 2012;6(2):137-192. https://doi.org/10.1007/s11682-012-9156-5
  • 18 Huisman TA, Schwamm LH, Schaefer PW, Koroshetz WJ, Shetty-Alva N, Ozsunar Y et al. Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. AJNR Am J Neuroradiol. 2004 Mar;25(3):370-6.
  • 19 Salmond CH, Menon DK, Chatfield DA, Williams GB, Pena A, Sahakian BJ et al. Diffusion tensor imaging in chronic head injury survivors: correlations with learning and memory indices. Neuroimage. 2006 Jan;29(1):117-24. https://doi.org/10.1016/j.neuroimage.2005.07.012
  • 20 Le Bihan D, Iima M. Diffusion magnetic resonance imaging: what water tells us about biological tissues. PLoS Biol. 2015 Jul;13(7):e1002203.https://doi.org/10.1371/journal.pbio.1002203
  • 21 Beaulieu C. The basis of anisotropic water diffusion in the nervous system: a technical review. NMR Biomed. 2002 Nov-Dec;15(7-8):435-55. https://doi.org/10.1002/nbm.782
  • 22 Karaarslan E, Arslan A. Diffusion weighted MR imaging in non-infarct lesions of the brain. Eur J Radiol. 2008 Mar;65(3):402-16. https://doi.org/10.1016/j.ejrad.2007.04.023PMID:17555903
  • 23 Le Bihan D. Apparent diffusion coefficient and beyond: what diffusion MR imaging can tell us about tissue structure. Radiology. 2013 Aug;268(2):318-22. https://doi.org/10.1148/radiol.13130420
  • 24 Ogura A, Hatano I, Osakabe K, Yamaguchi N, Koyama D, Watanabe H. Importance of fractional b value for calculating apparent diffusion coefficient in DWI. AJR Am J Roentgenol. 2016 Dec;207(6):1239-43. https://doi.org/10.2214/AJR.15.15945
  • 25 Mechtler LL, Shastri KK, Crutchfield KE. Advanced neuroimaging of mild traumatic brain injury. Neurol Clin. 2014 Feb;32(1):31-58. https://doi.org/10.1016/j.ncl.2013.08.002
  • 26 Nucifora PG, Verma R, Lee SK, Melhem ER. Diffusion-tensor MR imaging and tractography: exploring brain microstructure and connectivity. Radiology. 2007 Nov;245(2):367-84. https://doi.org/10.1148/radiol.2452060445
  • 27 Mori S, Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron. 2006 Sep;51(5):527-39. https://doi.org/10.1016/j.neuron.2006.08.012
  • 28 Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med. 1996 Dec;36(6):893-906. https://doi.org/10.1002/mrm.1910360612
  • 29 Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 2000 Oct;44(4):625-32.https://doi.org/10.1002/1522-2594(200010)44:4<625::AID-MRM17>3.0.CO;2-O
  • 30 Winston GP. The physical and biological basis of quantitative parameters derived from diffusion MRI. Quant Imaging Med Surg. 2012 Dec;2(4):254-65. https://doi.org/10.3978/j.issn.2223-4292.2012.12.05
  • 31 Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. 2002 Nov;17(3):1429-36. https://doi.org/10.1006/nimg.2002.1267PMID:12414282
  • 32 Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage. 2003 Nov;20(3):1714-22. https://doi.org/10.1016/j.neuroimage.2003.07.005
  • 33 Garin-Muga A, Borro D. Review and challenges of brain analysis through DTI measurements. Stud Health Technol Inform. 2014;207:27-36. https://doi.org/10.3233/978-1-61499-474-9-27
  • 34 Soares JM, Marques P, Alves V, Sousa N. A hitchhiker's guide to diffusion tensor imaging. Front Neurosci. 2013 Mar;7(31):31. https://doi.org/10.3389/fnins.2013.00031
  • 35 Snook L, Plewes C, Beaulieu C. Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment. Neuroimage. 2007 Jan;34(1):243-52. https://doi.org/10.1016/j.neuroimage.2006.07.021
  • 36 Mac Donald CL, Dikranian K, Bayly P, Holtzman D, Brody D. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J Neurosci. 2007 Oct;27(44):11869-76. https://doi.org/10.1523/JNEUROSCI.3647-07.2007
  • 37 Arfanakis K, Haughton VM, Carew JD, Rogers BP, Dempsey RJ, Meyerand ME. Diffusion tensor MR imaging in diffuse axonal injury. AJNR Am J Neuroradiol. 2002 May;23(5):794-802. https://doi.org/10.1016/j.neuroimage.2014.06.021
  • 38 Edlow BL, Copen WA, Izzy S, Bakhadirov K, Kouwe A, Glenn MB et al. Diffusion tensor imaging in acute-to-subacute traumatic brain injury: a longitudinal analysis. BMC Neurol. 2016 Jan;16:2. https://doi.org/10.1186/s12883-015-0525-8
  • 39 Mori S, van Zijl PC. Fiber tracking: principles and strategies - a technical review. NMR Biomed. 2002 Nov-Dec;15(7-8):468-80. https://doi.org/10.1002/nbm.781
  • 40 Tournier JD, Mori S, Leemans A. Diffusion tensor imaging and beyond. Magn Reson Med. 2011 Jun;65(6):1532-56. https://doi.org/10.1002/mrm.22924
  • 41 Wang JY, Bakhadirov K, Devous MD Sr, Abdi H, McColl R, Moore C et al. Diffusion tensor tractography of traumatic diffuse axonal injury. Arch Neurol. 2008 May;65(5):619-26. https://doi.org/10.1001/archneur.65.5.619
  • 42 Rutgers DR, Toulgoat F, Cazejust J, Fillard P, Lasjaunias P, Ducreux D. White matter abnormalities in mild traumatic brain injury: a diffusion tensor imaging study. AJNR Am J Neuroradiol. 2008 Mar;29(3):514-9. https://doi.org/10.3174/ajnr.A0856
  • 43 Brandstack N, Kurki T, Tenovuo O. Quantitative diffusiontensor tractography of long association tracts in patients with traumatic brain injury without associated findings at routine MR imaging. Radiology. 2013 Apr;267(1):231-9. https://doi.org/10.1148/radiol.12112570
  • 44 Yendiki A, Panneck P, Srinivasan P, Stevens A, Zöllei L, Augustinack J et al. Automated probabilistic reconstruction of white-matter pathways in health and disease using an atlas of the underlying anatomy. Front Neuroinform. 2011 Oct;5:23. https://doi.org/10.3389/fninf.2011.00023
  • 45 Koch SB, van Zuiden M, Nawijn L, Frijling JL, Veltman DJ, Olff M. Decreased uncinate fasciculus tract integrity in male and female patients with PTSD: a diffusion tensor imaging study. J Psychiatry Neurosci. 2017 Sep;42(5):331-42. https://doi.org/10.1503/jpn.160129
  • 46 Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006 Jul;31(4):1487-505. https://doi.org/10.1016/j.neuroimage.2006.02.024
  • 47 Bach M, Laun FB, Leemans A, Tax CM, Biessels GJ, Stieltjes B et al. Methodological considerations on tract-based spatial statistics (TBSS). Neuroimage. 2014 Oct;100:358-69. https://doi.org/10.1016/j.neuroimage.2014.06.021
  • 48 Zhang H, Yushkevich PA, Alexander DC, Gee JC. Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med Image Anal. 2006 Oct;10(5):764-85. https://doi.org/10.1016/j.media.2006.06.004
  • 49 Andrade CS, Conceição DM, Grassi DC et al. Evaluation of white matter integrity with tract-based spatial statistics in patients with traumatic brain injury. Vienna: European Society of Radiology; 2017. https://doi.org/10.1594/ecr2017/C-0747
  • 50 Chu Z, Wilde EA, Hunter JV, McCauley SR, Bigler ED, Troyanskaya M et al. Voxel-based analysis of diffusion tensor imaging in mild traumatic brain injury in adolescents. AJNR Am J Neuroradiol. 2010 Feb;31(2):340-6. https://doi.org/10.3174/ajnr.A1806
  • 51 Lipton ML, Gellella E, Lo C, Gold T, Ardekani BA, Shifteh K et al. Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. J Neurotrauma. 2008 Nov;25(11):1335-42. https://doi.org/10.1089/neu.2008.0547
  • 52 Xu J, Rasmussen IA, Lagopoulos J, Håberg A. Diffuse axonal injury in severe traumatic brain injury visualized using high-resolution diffusion tensor imaging. J Neurotrauma. 2007 May;24(5):753-65. https://doi.org/10.1089/neu.2006.0208