Longitudinal changes in brain volumetry and cognitive functions after moderate and severe diffuse axonal injury

References

• DiMaggio CJ, Avraham JB, Lee DC, Frangos SG, Wall SP. The epidemiology of emergency department trauma discharges in the United States. Acad Emerg Med. 2017;24:1244–56. doi:10.1111/acem.13223.
   PubMed Web of Science ®Google Scholar
• Vieira RC, Paiva WS, De Oliveira DV, Teixeira MJ, De Andrade AF, De Sousa RM. Diffuse axonal injury: epidemiology, outcome and associated risk factors. Front Neurol. 2016;7:178. doi:10.3389/fneur.2016.00178.
   PubMed Web of Science ®Google Scholar
• Corrigan JD, Selassie AW, Orman JA. The epidemiology of traumatic brain injury. J Head Trauma Rehabil. 2010;25:72–80. doi:10.1097/HTR.0b013e3181ccc8b4.
   PubMed Web of Science ®Google Scholar
• Corso P, Finkelstein E, Miller T, Fiebelkorn I, Zaloshnja E. Incidence and lifetime costs of injuries in the United States. Inj Prev. 2006;12:212–18. doi:10.1136/ip.2005.010983.
   PubMed Web of Science ®Google Scholar
• Zaninotto AL, Vicentini JE, Fregni F, Rodrigues PA, Botelho C, De Lucia MC, Paiva WS. Updates and current perspectives of psychiatric assessments after traumatic brain injury: a systematic review. Front Psychiatry. 2016;7:95. doi:10.3389/fpsyt.2016.00095.
   PubMed Web of Science ®Google Scholar
• McGinn MJ, Povlishock JT. Pathophysiology of traumatic brain injury. Neurosurg Clin N Am. 2016;27:397–407. doi:10.1016/j.nec.2016.06.002.
   PubMed Web of Science ®Google Scholar
• Shams S, Granberg T, Martola J, Charidimou A, Li X, Shams M, Fereshtehnejad SM, Cavallin L, Aspelin P, Wiberg-Kristoffersen M, et al. Cerebral microbleeds topography and cerebrospinal fluid biomarkers in cognitive impairment. J Cereb Blood Flow Metab. 2017;37:1006–13. doi:10.1177/0271678X16649401.
   PubMed Web of Science ®Google Scholar
• Ni J, Auriel E, Martinez-Ramirez S, Keil B, Reed AK, Fotiadis P, Gurol EM, Greenberg SM, Viswanathan A. Cortical localization of microbleeds in cerebral amyloid angiopathy: an ultra high-field 7T MRI study. J Alzheimers Dis. 2015;43:1325–30. doi:10.3233/JAD-140864.
   PubMed Web of Science ®Google Scholar
• Shively S, Scher AI, Perl DP, Diaz-Arrastia R. Dementia resulting from traumatic brain injury: what is the pathology? Arch Neurol. 2012;69:1245–51. doi:10.1001/archneurol.2011.3747.
   PubMed Web of Science ®Google Scholar
• Johnson VE, Stewart W, Smith DH. Traumatic brain injury and amyloid-β pathology: a link to Alzheimer’s disease? Nat Rev Neurosci. 2010;11:361–70. doi:10.1038/nrn2808.
   PubMed Web of Science ®Google Scholar
• Van den Heuvel C, Thornton E, Vink R. Traumatic brain injury and Alzheimer’s disease: a review. Prog Brain Res. 2007;161:303–16. doi:10.1016/S0079-6123(06)61021-2.
   PubMed Web of Science ®Google Scholar
• Jellinger KA. Head injury and dementia. Curr Opin Neurol. 2004;17:719–23.
   PubMed Web of Science ®Google Scholar
• Adle-Biassette H, Duyckaerts C, Wasowicz M, He Y, Fornes P, Foncin JF, Lecomte D, Hauw JJ. Beta AP deposition and head trauma. Neurobiol Aging. 1996;17:415–19.
   PubMed Web of Science ®Google Scholar
• Adrian H, Marten K, Salla N, Lasse V. Biomarkers of traumatic brain injury: temporal changes in body fluids. eNeuro. 2016;3. doi:10.1523/ENEURO.0294-16.2016.
   Web of Science ®Google Scholar
• Armstrong RC, Mierzwa AJ, Marion CM, Sullivan GM. White matter involvement after TBI: clues to axon and myelin repair capacity. Exp Neurol. 2016;275(Pt 3):328–33. doi:10.1016/j.expneurol.2015.02.011.
   PubMed Web of Science ®Google Scholar
• Kinoshita K. Traumatic brain injury: pathophysiology for neurocritical care. J Intensive Care. 2016;4:29. doi:10.1186/s40560-016-0138-3.
   PubMed Web of Science ®Google Scholar
• Povlishock JT, Katz DI. Update of neuropathology and neurological recovery after traumatic brain injury. J Head Trauma Rehabil. 2005;20:76–94.
   PubMed Web of Science ®Google Scholar
• Kato T, Nakayama N, Yasokawa Y, Okumura A, Shinoda J, Iwama T. Statistical image analysis of cerebral glucose metabolism in patients with cognitive impairment following diffuse traumatic brain injury. J Neurotrauma. 2007;24:919–26. doi:10.1089/neu.2006.0203.
   PubMed Web of Science ®Google Scholar
• Li S, Kuroiwa T, Ishibashi S, Sun L, Endo S, Ohno K. Transient cognitive deficits are associated with the reversible accumulation of amyloid precursor protein after mild traumatic brain injury. Neurosci Lett. 2006;409:182–86. doi:10.1016/j.neulet.2006.09.054.
   PubMed Web of Science ®Google Scholar
• Zaninotto AL, Vicentini JE, Solla DJ, Silva TT, Guirado VM, Feltrin F, De Lucia MC, Teixeira MJ, Paiva WS. Visuospatial memory improvement in patients with diffuse axonal injury (DAI): a 1-year follow-up study. Acta Neuropsychiatr. 2017;29:35–42. doi:10.1017/neu.2016.29.
   PubMed Web of Science ®Google Scholar
• Brezova V, Moen KG, Skandsen T, Vik A, Brewer JB, Salvesen O, Haberg AK. Prospective longitudinal MRI study of brain volumes and diffusion changes during the first year after moderate to severe traumatic brain injury. Neuroimage Clin. 2014;5:128–40. doi:10.1016/j.nicl.2014.03.012.
   PubMed Web of Science ®Google Scholar
• Green RE, Colella B, Maller JJ, Bayley M, Glazer J, Mikulis DJ. Scale and pattern of atrophy in the chronic stages of moderate-severe TBI. Front Hum Neurosci. 2014;8:67. doi:10.3389/fnhum.2014.00067.
   PubMed Web of Science ®Google Scholar
• Le K, Coelho C, Mozeiko J, Krueger F, Grafman J. Does brain volume loss predict cognitive and narrative discourse performance following traumatic brain injury? Am J Speech Lang Pathol. 2014;23:S271–84. doi:10.1044/2014_AJSLP-13-0095.
   PubMed Web of Science ®Google Scholar
• Ross DE, Ochs AL, Zannoni MD, Seabaugh JM. Alzheimer’s disease neuroimaging initiative. Back to the future: estimating pre-injury brain volume in patients with traumatic brain injury. Neuroimage. 2014;102(Pt 2):565–78. doi:10.1016/j.neuroimage.2014.07.043.
   PubMed Web of Science ®Google Scholar
• Farbota KD, Sodhi A, Bendlin BB, McLaren DG, Xu G, Rowley HA, Johnson SC. Longitudinal volumetric changes following traumatic brain injury: a tensor-based morphometry study. J Int Neuropsychol Soc. 2012;18:1006–18. doi:10.1017/S1355617712000835.
   PubMed Web of Science ®Google Scholar
• Moen KG, Skandsen T, Folvik M, Brezova V, Kvistad KA, Rydland J, Manley GT, Vik A. A longitudinal MRI study of traumatic axonal injury in patients with moderate and severe traumatic brain injury. J Neurol Neurosurg Psychiatry. 2012;83:1193–200. doi:10.1136/jnnp-2012-302644.
   PubMed Web of Science ®Google Scholar
• Irimia A, Chambers MC, Alger JR, Filippou M, Prastawa MW, Wang B, Hovda DA, Gerig G, Toga AW, Kikinis R, et al. Comparison of acute and chronic traumatic brain injury using semi-automatic multimodal segmentation of MR volumes. J Neurotrauma. 2011;28:2287–306. doi:10.1089/neu.2011.1920.
   PubMed Web of Science ®Google Scholar
• Warner MA, Youn TS, Davis T, Chandra A, Marquez de La Plata C, Moore C, Harper C, Madden CJ, Spence J, McColl R, et al. Regionally selective atrophy after traumatic axonal injury. Arch Neurol. 2010;67:1336–44. doi:10.1001/archneurol.2010.149.
   PubMed Web of Science ®Google Scholar
• Sidaros A, Skimminge A, Liptrot MG, Sidaros K, Engberg AW, Herning M, Paulson OB, Jernigan TL, Rostrup E. Long-term global and regional brain volume changes following severe traumatic brain injury: a longitudinal study with clinical correlates. Neuroimage. 2009;44:1–8. doi:10.1016/j.neuroimage.2008.08.030.
   PubMed Web of Science ®Google Scholar
• Ma J, Zhang K, Wang Z, Chen G. Progress of research on diffuse axonal injury after traumatic brain injury. Neural Plast. 2016;2016:9746313. doi:10.1155/2016/9746313.
   PubMed Web of Science ®Google Scholar
• Warner MA, Marquez de La Plata C, Spence J, Wang JY, Harper C, Moore C, Devous M, Diaz-Arrastia R. Assessing spatial relationships between axonal integrity, regional brain volumes, and neuropsychological outcomes after traumatic axonal injury. J Neurotrauma. 2010;27:2121–30. doi:10.1089/neu.2010.1429.
   PubMed Web of Science ®Google Scholar
• Ding K, Marquez de La Plata C, Wang JY, Mumphrey M, Moore C, Harper C, Madden CJ, McColl R, Whittemore A, Devous MD, et al. Cerebral atrophy after traumatic white matter injury: correlation with acute neuroimaging and outcome. J Neurotrauma. 2008;25:1433–40. doi:10.1089/neu.2008.0683.
   PubMed Web of Science ®Google Scholar
• Hurley RA, McGowan JC, Arfanakis K, Taber KH. Traumatic axonal injury: novel insights into evolution and identification. J Neuropsychiatry Clin Neurosci. 2004;16:1–7. doi:10.1176/jnp.16.1.1.
   PubMed Web of Science ®Google Scholar
• Gentry LR, Godersky JC, Thompson B. MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. AJR Am J Roentgenol. 1988;150:663–72. doi:10.2214/ajr.150.3.663.
   PubMed Web of Science ®Google Scholar
• Liu J, Kou Z, Tian Y. Diffuse axonal injury after traumatic cerebral microbleeds: an evaluation of imaging techniques. Neural Regen Res. 2014;9:1222–30. doi:10.4103/1673-5374.135330.
   PubMed Web of Science ®Google Scholar
• Liu T, Surapaneni K, Lou M, Cheng L, Spincemaille P, Wang Y. Cerebral microbleeds: burden assessment by using quantitative susceptibility mapping. Radiology. 2012;262:269–78. doi:10.1148/radiol.11110251.
   PubMed Web of Science ®Google Scholar
• Toth A, Kornyei B, Kovacs N, Rostas T, Buki A, Doczi T, Bogner P, Schwarcz A. Both hemorrhagic and non-hemorrhagic traumatic MRI lesions are associated with the microstructural damage of the normal appearing white matter. Behav Brain Res. 2017. doi:10.1016/j.bbr.2017.02.039.
   Web of Science ®Google Scholar
• Kenney K, Amyot F, Haber M, Pronger A, Bogoslovsky T, Moore C, Diaz-Arrastia R. Cerebral vascular injury in traumatic brain injury. Exp Neurol. 2016;275(Pt 3):353–66. doi:10.1016/j.expneurol.2015.05.019.
   PubMed Web of Science ®Google Scholar
• Moenninghoff C, Kraff O, Maderwald S, Umutlu L, Theysohn JM, Ringelstein A, Wrede KH, Deuschl C, Altmeppen J, Ladd ME, et al. Diffuse axonal injury at ultra-high field MRI. PLoS One. 2015;10:e0122329. doi:10.1371/journal.pone.0122329.
   PubMed Web of Science ®Google Scholar
• Toth A, Kovacs N, Perlaki G, Orsi G, Aradi M, Komaromy H, Ezer E, Bukovics P, Farkas O, Janszky J, et al. Multi-modal magnetic resonance imaging in the acute and sub-acute phase of mild traumatic brain injury: can we see the difference? J Neurotrauma. 2013;30:2–10. doi:10.1089/neu.2012.2486.
   PubMed Web of Science ®Google Scholar
• Mez J, Stern RA, McKee AC. Chronic traumatic encephalopathy: where are we and where are we going? Curr Neurol Neurosci Rep. 2013;13:407. doi:10.1007/s11910-013-0407-7.
   PubMed Web of Science ®Google Scholar
• Wright MJ, McArthur DL, Alger JR, Van Horn J, Irimia A, Filippou M, Glenn TC, Hovda DA, Vespa P. Early metabolic crisis-related brain atrophy and cognition in traumatic brain injury. Brain Imaging Behav. 2013;7:307–15. doi:10.1007/s11682-013-9231-6.
   PubMed Web of Science ®Google Scholar
• Bendlin BB, Ries ML, Lazar M, Alexander AL, Dempsey RJ, Rowley HA, Sherman JE, Johnson SC. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage. 2008;42:503–14. doi:10.1016/j.neuroimage.2008.04.254.
   PubMed Web of Science ®Google Scholar
• Irimia A, Goh SY, Torgerson CM, Vespa P, Van Horn JD. Structural and connectomic neuroimaging for the personalized study of longitudinal alterations in cortical shape, thickness and connectivity after traumatic brain injury. J Neurosurg Sci. 2014;58:129–44.
   PubMed Web of Science ®Google Scholar
• Van den Heuvel TL, Van Der Eerden AW, Manniesing R, Ghafoorian M, Tan T, Andriessen TM, Vande Vyvere T, Van den Hauwe L, Ter Haar Romeny BM, Goraj BM, et al. Automated detection of cerebral microbleeds in patients with traumatic brain injury. Neuroimage Clin. 2016;12:241–51. doi:10.1016/j.nicl.2016.07.002.
   PubMed Web of Science ®Google Scholar
• Yates PA, Villemagne VL, Ellis KA, Desmond PM, Masters CL, Rowe CC. Cerebral microbleeds: a review of clinical, genetic, and neuroimaging associations. Front Neurol. 2014;4:205. doi:10.3389/fneur.2013.00205.
   PubMed Web of Science ®Google Scholar
• Marshall LF, Marshall SB, Klauber MR, Van Berkum Clark M, Eisenberg H, Jane JA, Luerssen TG, Marmarou A, Foulkes MA. The diagnosis of head injury requires a classification based on computed axial tomography. J Neurotrauma. 1992;9(Suppl 1):S287–92.
   PubMed Web of Science ®Google Scholar
• Gregoire SM, Chaudhary UJ, Brown MM, Yousry TA, Kallis C, Jager HR, Werring DJ. The microbleed anatomical rating scale (MARS): reliability of a tool to map brain microbleeds. Neurology. 2009;73:1759–66. doi:10.1212/WNL.0b013e3181c34a7d.
   PubMed Web of Science ®Google Scholar
• Maclaren J, Han Z, Vos SB, Fischbein N, Bammer R. Reliability of brain volume measurements: a test-retest dataset. Sci Data. 2014;1:140037. doi:10.1038/sdata.2014.37.
   PubMed Web of Science ®Google Scholar
• Jovicich J, Marizzoni M, Sala-Llonch R, Bosch B, Bartres-Faz D, Arnold J, Benninghoff J, Wiltfang J, Roccatagliata L, Nobili F, et al. Brain morphometry reproducibility in multi-center 3T MRI studies: a comparison of cross-sectional and longitudinal segmentations. Neuroimage. 2013;83:472–84. doi:10.1016/j.neuroimage.2013.05.007.
   PubMed Web of Science ®Google Scholar
• Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999;9:179–94. doi:10.1006/nimg.1998.0395.
   PubMed Web of Science ®Google Scholar
• Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage. 1999;9:195–207. doi:10.1006/nimg.1998.0396.
   PubMed Web of Science ®Google Scholar
• Reuter M, Schmansky NJ, Rosas HD, Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage. 2012;61:1402–18. doi:10.1016/j.neuroimage.2012.02.084.
   PubMed Web of Science ®Google Scholar
• Reuter M, Rosas HD, Fischl B. Highly accurate inverse consistent registration: a robust approach. Neuroimage. 2010;53:1181–96. doi:10.1016/j.neuroimage.2010.07.020.
   PubMed Web of Science ®Google Scholar
• Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86:420–28.
   PubMed Web of Science ®Google Scholar
• Ross DE. Review of longitudinal studies of MRI brain volumetry in patients with traumatic brain injury. Brain Inj. 2011;25:1271–78. doi:10.3109/02699052.2011.624568.
   PubMed Web of Science ®Google Scholar
• Xu Y, McArthur DL, Alger JR, Etchepare M, Hovda DA, Glenn TC, Huang S, Dinov I, Vespa PM. Early nonischemic oxidative metabolic dysfunction leads to chronic brain atrophy in traumatic brain injury. J Cereb Blood Flow Metab. 2010;30:883–94. doi:10.1038/jcbfm.2009.263.
   PubMed Web of Science ®Google Scholar
• Trivedi MA, Ward MA, Hess TM, Gale SD, Dempsey RJ, Rowley HA, Johnson SC. Longitudinal changes in global brain volume between 79 and 409 days after traumatic brain injury: relationship with duration of coma. J Neurotrauma. 2007;24:766–71. doi:10.1089/neu.2006.0205.
   PubMed Web of Science ®Google Scholar
• Palacios EM, Sala-Llonch R, Junque C, Fernandez-Espejo D, Roig T, Tormos JM, Bargallo N, Vendrell P. Long-term declarative memory deficits in diffuse TBI: correlations with cortical thickness, white matter integrity and hippocampal volume. Cortex. 2013;49:646–57. doi:10.1016/j.cortex.2012.02.011.
   PubMed Web of Science ®Google Scholar
• Maxwell WL, Povlishock JT, Graham DL. A mechanistic analysis of nondisruptive axonal injury: a review. J Neurotrauma. 1997;14:419–40. doi:10.1089/neu.1997.14.419.
   PubMed Web of Science ®Google Scholar
• Adams JH, Doyle D, Ford I, Gennarelli TA, Graham DI, McLellan DR. Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology. 1989;15:49–59.
   PubMed Web of Science ®Google Scholar
• Vakil E. The effect of moderate to severe traumatic brain injury (TBI) on different aspects of memory: a selective review. J Clin Exp Neuropsychol. 2005;27:977–1021. doi:10.1080/13803390490919245.
   PubMed Web of Science ®Google Scholar
• Kersel DA, Marsh NV, Havill JH, Sleigh JW. Neuropsychological functioning during the year following severe traumatic brain injury. Brain Inj. 2001;15:283–96. doi:10.1080/02699050010005887.
   PubMed Web of Science ®Google Scholar
• Martin RM, Wright MJ, Lutkenhoff ES, Ellingson BM, Van Horn JD, Tubi M, Alger JR, McArthur DL, Vespa PM. Traumatic hemorrhagic brain injury: impact of location and resorption on cognitive outcome. J Neurosurg. 2017;126:796–804. doi:10.3171/2016.3.JNS151781.
   PubMed Web of Science ®Google Scholar
• Rabinowitz AR, Hart T, Whyte J, Kim J. Neuropsychological recovery trajectories in moderate to severe traumatic brain injury: influence of patient characteristics and diffuse axonal injury. J Int Neuropsychological Soc. 2018;24:237–46. doi:10.1017/s1355617717000996.
   PubMed Web of Science ®Google Scholar
• Witte OW, Stoll G. Delayed and remote effects of focal cortical infarctions: secondary damage and reactive plasticity. Adv Neurol. 1997;73:207–27.
   PubMedGoogle Scholar
• Cramer SC. Stroke recovery: how the computer reprograms itself. Neuronal plasticity: the key to stroke recovery. Kananskis, Alberta, Canada, 19-22 March 2000. Mol Med Today England. 2000;6:301–03. doi:10.1016/S1357-4310(00)01744-5.
   PubMedGoogle Scholar
• Jones TA, Chu CJ, Grande LA, Gregory AD. Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J Neurosci. 1999;19:10153–63.
   PubMed Web of Science ®Google Scholar
• Kleim JA, Freeman JH Jr., Bruneau R, Nolan BC, Cooper NR, Zook A, Walters D. Synapse formation is associated with memory storage in the cerebellum. Proc Natl Acad Sci U S A. 2002;99:13228–31. doi:10.1073/pnas.202483399.
   PubMed Web of Science ®Google Scholar
• Nudo RJ. Recovery after brain injury: mechanisms and principles. Front Hum Neurosci. 2013;7. doi:10.3389/fnhum.2013.00887.
   PubMed Web of Science ®Google Scholar
• Toth A, Kovacs N, Tamas V, Kornyei B, Nagy M, Horvath A, Rostas T, Bogner P, Janszky J, Doczi T, et al. Microbleeds may expand acutely after traumatic brain injury. Neurosci Lett. 2016;617:207–12. doi:10.1016/j.neulet.2016.02.028.
   PubMed Web of Science ®Google Scholar
• Watanabe J, Maruya J, Kanemaru Y, Miyauchi T, Nishimaki K. Transient disappearance of microbleeds in the subacute period based on T2*-weighted gradient echo imaging in traumatic brain injury. Acta Neurochir (Wien). 2016;158:1247–50. doi:10.1007/s00701-016-2805-5.
   PubMed Web of Science ®Google Scholar