Diffusion tensor imaging reveals acute subcortical changes after mild blast-induced traumatic brain injury

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Kamnaksh, Alaa ^a   Budde, Matthew D ^b,e   Kovesdi, Erzsebet ^c   Long, Joseph B ^d   Frank, Joseph A ^b   Agoston, Denes V ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

^c DEPARTMENT OF VETERANS AFFAIRS   (United States)

^d WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^e MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BRAIN; BRAIN INJURIES; DIFFUSION TENSOR IMAGING; HIPPOCAMPUS; MALE; ORGAN SIZE; PATHOLOGY; RAT; TIME;

ANIMALS; BRAIN; BRAIN INJURIES; DIFFUSION TENSOR IMAGING; HIPPOCAMPUS; MALE; ORGAN SIZE; RATS; TIME FACTORS;

EID: 84899864979     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep04809     Document Type: Article

References (59)

1. Laker, S. R. Epidemiology of concussion andmild traumatic brain injury. PM R 3, S354-358; DOI:10.1016/j.pmrj.2011.07.017 (2011).
2. Hendricks, A. M. et al. Screening for mild traumatic brain injury in OEF-OIF deployed US military: an empirical assessment of VHA's experience. Brain. Inj. 27, 125-134; DOI:10.3109/02699052.2012.729284 (2013).
3. Vanderploeg, R. D. et al. Health outcomes associated with military deployment: mild traumatic brain injury, blast, trauma, and combat associations in the Florida National Guard. Arch. Phys. Med. Rehabil. 93, 1887-1895; DOI:10.1016/j.apmr.2012.05.024 (2012).
4. Xydakis, M. S., Ling, G. S., Mulligan, L. P., Olsen, C. H. & Dorlac, W. C. Epidemiologic aspects of traumatic brain injury in acute combat casualties at a major military medical center: a cohort study. Ann. Neurol. 72, 673-681; DOI:10.1002/ana.23757 (2012).
5. Brenner, L. A., Vanderploeg, R. D. & Terrio, H. Assessment and diagnosis of mild traumatic brain injury, posttraumatic stress disorder, and other polytrauma conditions: burden of adversity hypothesis. Rehabil. Psychol. 54, 239-246; DOI:10.1037/a0016908 (2009).
6. Stern, R. A. et al. Long-term consequences of repetitive brain trauma: chronic traumatic encephalopathy. PM R 3, S460-467; DOI:10.1016/j.pmrj.2011.08. 008 (2011).
7. Aoki, Y., Inokuchi, R., Gunshin, M., Yahagi, N. & Suwa, H. Diffusion tensor imaging studies of mild traumatic brain injury: a meta-analysis. J. Neurol. Neurosurg. Psychiatry 83, 870-876; DOI:10.1136/jnnp-2012-302742 (2012).
8. Shenton, M. E. et al. A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav. 6, 137-192; DOI:10.1007/s11682-012-9156-5 (2012).
9. Voelbel, G. T., Genova, H. M., Chiaravalotti, N. D. & Hoptman, M. J. Diffusion tensor imaging of traumatic brain injury review: implications for neurorehabilitation. NeuroRehabilitation 31, 281-293; DOI:10.3233/nre-2012-0796 (2012).
10. Xiong, K. L., Zhu, Y. S. & Zhang, W. G. Diffusion tensor imaging and magnetic resonance spectroscopy in traumatic brain injury: a review of recent literature. Brain Imaging Behav. DOI:10.1007/s11682-013-9288-2 (2014).
11. Benzinger, T. L. et al. Blast-related brain injury: imaging for clinical and research applications: report of the 2008 st. Louis workshop. J. Neurotrauma 26, 2127-2144; DOI:10.1089/neu.2009-0885 (2009).
12. Levin, H. S. et al. Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. J. Neurotrauma 27, 683-694; DOI:10.1089/neu.2009.1073 (2010).
13. Mendez, M. F. et al. Mild traumatic brain injury from primary blast vs. blunt forces: post-concussion consequences and functional neuroimaging. NeuroRehabilitation 32, 397-407; DOI:10.3233/nre-130861 (2013).
14. Petrie, E. C. et al. Neuroimaging, behavioral, and psychological sequelae of repetitive combined blast/impact mild traumatic brain injury in Iraq and Afghanistan war veterans. J. Neurotrauma 31, 425-436; DOI:10.1089/neu.2013.2952 (2014).
15. Matthews, S. C. et al. A multimodal imaging study in U.S. veterans of Operations Iraqi and Enduring Freedom with and without major depression after blastrelated concussion. Neuroimage 54, S69-75; DOI:10.1016/j.neuroimage.2010. 04.269 (2011).
16. Mac Donald, C. et al. Cerebellar white matter abnormalities following primary blast injury in US military personnel. PLoS ONE 8, e55823; DOI:10.1371/journal.pone.0055823 (2013).
17. Matthews, S. C., Spadoni, A. D., Lohr, J. B., Strigo, I. A. & Simmons, A. N. 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. 204, 149-154; DOI:10.1016/j.pscychresns.2012.04.018 (2012).
18. Bennett, R. E., Mac Donald, C. L. & Brody, D. L. Diffusion tensor imaging detects axonal injury in a mouse model of repetitive closed-skull traumatic brain injury. Neurosci. Lett. 513, 160-165; DOI:10.1016/j.neulet.2012. 02.024 (2012).
19. Albensi, B. C. et al. Diffusion and high resolution MRI of traumatic brain injury in rats: time course and correlation with histology. Exp. Neurol. 162, 61-72; DOI:10.1006/exnr.2000.7256 (2000).
20. Cernak, I. et al. The pathobiology of moderate diffuse traumatic brain injury as identified using a new experimental model of injury in rats. Neurobiol. Dis. 17, 29-43; DOI:10.1016/j.nbd.2004.05.011 (2004).
21. Henninger, N. et al. Differential recovery of behavioral status and brain function assessed with functional magnetic resonance imaging after mild traumatic brain injury in the rat. Crit. Care Med. 35, 2607-2614; DOI:10.1097/01.ccm.0000286395.79654.8d (2007).
22. van de Looij, Y. et al. Diffusion tensor imaging of diffuse axonal injury in a rat brain trauma model. NMR Biomed. 25, 93-103; DOI:10.1002/nbm.1721 (2012).
23. Budde, M. D. et al. Primary blast traumatic brain injury in the rat: relating diffusion tensor imaging and behavior. Front. Neurol. 4, 154; DOI:10.3389/fneur.2013.00154 (2013).
24. Calabrese, E. et al. Diffusion tensor imaging reveals white matter injury in a rat model of repetitive blast-induced traumatic brain injury. J. Neurotrauma. DOI:10.1089/neu.2013.3144 (2014).
25. Morey, R. A. et al. Effects of chronic mild traumatic brain injury on white matter integrity in Iraq and Afghanistan war veterans. Hum. Brain Mapp. 34, 2986-2999; DOI:10.1002/hbm.22117 (2013).
26. Di Battista, A. P., Rhind, S. G. & Baker, A. J. Application of blood-based biomarkers in human mild traumatic brain injury. Front. Neurol. 4, 44; DOI:10.3389/fneur.2013.00044 (2013).
27. Kobeissy, F. H. et al. Neuroproteomics and systems biology-based discovery of protein biomarkers for traumatic brain injury and clinical validation. Proteomics Clin. Appl. 2, 1467-1483; DOI:10.1002/prca.200800011 (2008).
28. Wang, K. K. et al. Proteomic identification of biomarkers of traumatic brain injury. Expert Rev. Proteomics 2, 603-614; DOI:10.1586/14789450.2.4.603 (2005).
29. Agoston, D. V., Risling, M. & Bellander, B. M. Bench-to-bedside and bedside back to the bench; coordinating clinical and experimental traumatic brain injury studies. Front. Neurol. 3, 3; DOI:10.3389/fneur.2012.00003 (2012).
30. Kwon, S. K. et al. Stress and traumatic brain injury: a behavioral, proteomics, and histological study. Front. Neurol. 2, 12; DOI:10.3389/fneur. 2011.00012 (2011).
31. Kamnaksh, A. et al. Factors affecting blast traumatic brain injury. J. Neurotrauma 28, 2145-2153; DOI:10.1089/neu.2011.1983 (2011).
32. Kovesdi, E. et al. The effect of enriched environment on the outcome of traumatic brain injury; a behavioral, proteomics, and histological study. Front. Neurosci. 5, 42; DOI:10.3389/fnins.2011.00042 (2011).
33. Kovesdi, E. et al. Acute minocycline treatment mitigates the symptoms of mild blast-induced traumatic brain injury. Front. Neurol. 3, 111; DOI:10.3389/fneur.2012.00111 (2012).
34. Orrison, W.W. et al. Traumatic brain injury: a review and high-field MRI findings in 100 unarmed combatants using a literature-based checklist approach. J. Neurotrauma 26, 689-701; DOI:10.1089/neu.2008.0636 (2009).
35. Bigler, E. D. Quantitative magnetic resonance imaging in traumatic brain injury. J. Head Trauma Rehabil. 16, 117-134 (2001).
36. Kamnaksh, A. et al. Neurobehavioral, cellular, and molecular consequences of single and multiple mild blast exposure. Electrophoresis 33, 3680-3692; DOI:10.1002/elps.201200319 (2012).
37. Ahmed, F. et al. Time-dependent changes of protein biomarker levels in the cerebrospinal fluid after blast traumatic brain injury. Electrophoresis 33, 3705-3711; DOI:10.1002/elps.201200299 (2012).
38. Hetherington, H. P. et al. MRSI of the medial temporal lobe at 7 T in explosive blast mild traumatic brain injury. Magn. Reson. Med. 71, 1358-1367; DOI:10.1002/mrm.24814 (2014).
39. Masel, B. E. et al. Galveston Brain Injury Conference 2010: clinical and experimental aspects of blast injury. J. Neurotrauma 29, 2143-2171; DOI:10.1089/neu.2011.2258 (2012).
40. Scheibel, R. S. et al. Altered brain activation in military personnel with one or more traumatic brain injuries following blast. J. Int. Neuropsychol. Soc. 18, 89-100; DOI:10.1017/s1355617711001433 (2012).
41. Lu, H. et al. Registering and analyzing rat fMRI data in the stereotaxic framework by exploiting intrinsic anatomical features. Magn. Reson. Imaging 28, 146-152; DOI:10.1016/j.mri.2009.05.019 (2010).
42. Goldstein, L. E. et al. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci. Transl. Med. 4, 134ra60; DOI:10.1126/scitranslmed.3003716 (2012).
43. Jorge, R. E. et al. Whitematter abnormalities in veterans with mild traumatic brain injury. Am. J. Psychiatry 169, 1284-1291; DOI:10.1176/appi.ajp. 2012.12050600 (2012).
44. Stoodley, C. J. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum 11, 352-365; DOI:10.1007/s12311-011-0260-7 (2012).
45. VanOverwalle, F., Baetens, K., Marien, P. & Vandekerckhove, M. Social cognition and the cerebellum: A meta-analysis of over 350 fMRI studies. Neuroimage 86, 554-572; DOI:10.1016/j.neuroimage.2013.09.033 (2014).
46. Crestani, C. C. et al. Mechanisms in the bed nucleus of the stria terminalis involved in control of autonomic and neuroendocrine functions: a review. Curr. Neuropharmacol. 11, 141-159; DOI:10.2174/1570159x11311020002 (2013).
47. Rodrigo, J. et al. Physiology and pathophysiology of nitric oxide in the nervous system, with special mention of the islands of Calleja and the circunventricular organs. Histol. Histopathol. 17, 973-1003 (2002).
48. Bass, C. R. et al. Brain injuries from blast. Ann. Biomed. Eng. 40, 185-202; DOI:10.1007/s10439-011-0424-0 (2012).
49. Ahmed, F. A., Kamnaksh, A., Kovesdi, E., Long, J. B. & Agoston, D. V. Long-term consequences of single and multiple mild blast exposure on select physiological parameters and blood-based biomarkers. Electrophoresis 34, 2229-2233; DOI:10.1002/elps.201300077 (2013).
50. Long, J. B. et al. Blast overpressure in rats: recreating a battlefield injury in the laboratory. J. Neurotrauma 26, 827-840; DOI:10.1089/neu.2008.0748 (2009).
51. Hasan, K. M., Parker, D. L. & Alexander, A. L. Comparison of gradient encoding schemes for diffusion-tensor MRI. J. Magn. Reson. Imaging 13, 769-780 (2001).
52. Budde, M. D. & Frank, J. A. Examining brain microstructure using structure tensor analysis of histological sections. Neuroimage 63, 1-10, DOI:10.1016/j.neuroimage.2012.06.042 (2012).
53. Budde, M. D., Janes, L., Gold, E., Turtzo, L. C. & Frank, J. A. The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: validation in the rat using Fourier analysis of stained tissue sections. Brain 134, 2248-2260; DOI:10.1093/brain/awr161 (2011).
54. Zhang, H., Yushkevich, P. A., Alexander, D. C. & Gee, J. C. Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med. Image Anal. 10, 764-785; DOI:10.1016/j.media.2006.06.004 (2006).
55. Adluru, N. et al. A diffusion tensor brain template for rhesus macaques. Neuroimage 59, 306-318; DOI:10.1016/j.neuroimage.2011.07.029 (2012).
56. Ferris, C. F. et al. Functional magnetic resonance imaging in awake animals. Rev. Neurosci. 22, 665-674; DOI:10.1515/rns.2011.050 (2011).
57. Paxinos, G. & Watson, C. The Rat Brain in Stereotactic Coordinates. (Academic Press, 2007).
58. Avants, B. B. et al. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage, 54, 2033-2044; DOI:10.1016/j.neuroimage.2010.09.025 (2011).
59. Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N. & Golani, I. Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 125, 279-284 (2001).