Neuroimaging, behavioral, and psychological sequelae of repetitive combined blast/impact mild traumatic brain injury in Iraq and Afghanistan war veterans

Journal of Neurotrauma

Volumn 31, Issue 5, 2014, Pages 425-436

  Petrie, Eric C ^a,b   Cross, Donna J ^b   Yarnykh, Vasily L ^b   Richards, Todd ^b   Martin, Nathalie M ^b   Pagulayan, Kathleen ^a,b   Hoff, David ^a   Hart, Kim ^a   Mayer, Cynthia ^a   Tarabochia, Matthew ^a   Raskind, Murray A ^a,b   Minoshima, Satoshi ^b   Peskind, Elaine R ^a,b  

^a VA Puget Sound   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

diffusion tensor imaging; macromolecular proton fraction; mild traumatic brain injury; positron emission tomography; veterans

Indexed keywords

FLUORODEOXYGLUCOSE F 18;

ADULT; AFGHANISTAN; ALCOHOL CONSUMPTION; ARTICLE; BEHAVIORAL SCIENCE; BRAIN METABOLISM; CLINICAL ARTICLE; DEPRESSION; FRACTIONAL ANISOTROPY; GLUCOSE METABOLISM; GRAY MATTER; HUMAN; IRAQ; MALE; MIDDLE AGED; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; POSTTRAUMATIC STRESS DISORDER; SELF REPORT; SLEEP DISORDER; STRUCTURED CLINICAL INTERVIEW FOR DSM DISORDERS; TRAUMATIC BRAIN INJURY; VETERAN;

ADULT; AFGHAN CAMPAIGN 2001-; ANISOTROPY; BLAST INJURIES; BRAIN INJURIES; FEMALE; HUMANS; IRAQ WAR, 2003-2011; MALE; MENTAL DISORDERS; MIDDLE AGED; NERVE FIBERS, MYELINATED; NEUROIMAGING; NEUROPSYCHOLOGICAL TESTS; STRESS DISORDERS, POST-TRAUMATIC; VETERANS; YOUNG ADULT;

EID: 84896898721     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2013.2952     Document Type: Article

References (71)

1. Kay, T., Harrington, D.E., Adams, R., Anderson, T., Berrol, S., Cicerone, K., Dahlberg, C., Gerber, D., Goka, R., Harley, P., Hilt, J., Horn, L., Lehmkuhl, D., and Malec, J. (1993). Definition of mild traumatic brain injury. J. Head Trauma Rehabil. 8, 86-87.
2. Goldstein, L.E., Fisher, A.M., Tagge, C.A., Zhang, X.L., Velisek, L., Sullivan, J.A., Upreti, C., Kracht, J.M., Ericsson, M., Wojnarowicz, M.W., Goletiani, C.J., Maglakelidze, G.M., Casey, N., Moncaster, J.A., Minaeva, O., Moir, R.D., Nowinski, C.J., Stern, R.A., Cantu, R.C., Geiling, J., Blusztajn, J.K., Wolozin, B.L., Ikezu, T., Stein, T.D., Budson, A.E., Kowall, N.W., Chargin, D., Sharon, A., Saman, S., Hall, G.F., Moss, W.C., Cleveland, R.O., Tanzi, R.E., Stanton, P.K., and McKee, A.C. (2012). Chronic traumatic encephalopathy in blastexposed military veterans and a blast neurotrauma mouse model. Sci. Transl. Med. 4, 134ra160.
3. McKee, A.C., Stern, R.A., Nowinski, C.J., Stein, T.D., Alvarez, V.E., Daneshvar, D.H., Lee, H.S., Wojtowicz, S.M., Hall, G., Baugh, C.M., Riley, D.O., Kubilus, C.A., Cormier, K.A., Jacobs, M.A., Martin, B.R., Abraham, C.R., Ikezu, T., Reichard, R.R., Wolozin, B.L., Budson, A.E., Goldstein, L.E., Kowall, N.W., and Cantu, R.C. (2013). The spectrum of disease in chronic traumatic encephalopathy. Brain 136, 43-64.
4. Omalu, B., Hammers, J.L., Bailes, J., Hamilton, R.L., Kamboh, M.I., Webster, G., and Fitzsimmons, R.P. (2011). Chronic traumatic encephalopathy in an Iraqi war veteran with posttraumatic stress disorder who committed suicide. Neurosurg. Focus 31, E3.
5. Davenport, N.D., Lim, K.O., Armstrong, M.T., and Sponheim, S.R. (2012). Diffuse and spatially variable white matter disruptions are associated with blast-related mild traumatic brain injury. Neuroimage 59, 2017-2024.
6. Jorge, R.E., Acion, L., White, T., Tordesillas-Gutierrez, D., Pierson, R., Crespo-Facorro, B., and Magnotta, V.A. (2012). White matter abnormalities in veterans with mild traumatic brain injury. Am. J. Psychiatry 169, 1284-1291.
7. Levin, H.S., Wilde, E., Troyanskaya, M., Petersen, N.J., Scheibel, R., Newsome, M., Radaideh, M., Wu, T., Yallampalli, R., Chu, Z., and Li, X. (2010). Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. J. Neurotrauma 27, 683-694.
8. Mac Donald, C.L., Johnson, A.M., Cooper, D., Nelson, E.C., Werner, N.J., Shimony, J.S., Snyder, A.Z., Raichle, M.E., Witherow, J.R., Fang, R., Flaherty, S.F., and Brody, D.L. (2011). Detection of blastrelated traumatic brain injury in U.S. military personnel. N. Engl. J. Med. 364, 2091-2100.
9. Morey, R.A., Haswell, C.C., Selgrade, E.S., Massoglia, D., Liu, C., Weiner, J., Marx, C.E.; MIRECC Work Group, Cernak, I., McCarthy, G. (2013). Effects of chronic mild traumatic brain injury on white matter integrity in Iraq and Afghanistan war Veterans. Hum. Brain Mapp. 34, 2986-2999.
10. Peskind, E.R., Petrie, E.C., Cross, D.J., Pagulayan, K., McCraw, K., Hoff, D., Hart, K., Yu, C.E., Raskind, M.A., Cook, D.G., and Minoshima, S. (2011). Cerebrocerebellar hypometabolism associated with repetitive blast exposure mild traumatic brain injury in 12 Iraq war Veterans with persistent post-concussive symptoms. Neuroimage 54, S76-S82.
11. Underhill, H.R., Rostomily, R.C., Mikheev, A.M., Yuan, C., and Yarnykh, V.L. (2011). Fast bound pool fraction imaging of the in vivo rat brain: Association with myelin content and validation in the C6 glioma model. Neuroimage 54, 2052-2065.
12. Underhill, H.R., Yuan, C., and Yarnykh, V.L. (2009). Direct quantitative comparison between cross-relaxation imaging and diffusion tensor imaging of the human brain at 3.0 T. Neuroimage 47, 1568-1578.
13. Yarnykh, V.L., and Yuan, C. (2004). Cross-relaxation imaging reveals detailed anatomy of white matter fiber tracts in the human brain. Neuroimage 23, 409-424.
14. Yarnykh, V.L. (2012). Fast macromolecular proton fraction mapping from a single off-resonance magnetization transfer measurement. Magn. Reson. Med. 68, 166-178.
15. Rausch, M., Tofts, P., Lervik, P., Walmsley, A., Mir, A., Schubart, A., and Seabrook, T. (2009). Characterization of white matter damage in animal models of multiple sclerosis by magnetization transfer ratio and quantitative mapping of the apparent bound proton fraction f. Mult. Scler. 15, 16-27.
16. Samsonov, A., Alexander, A.L., Mossahebi, P., Wu, Y.C., Duncan, I.D., and Field, A.S. (2012). Quantitative MR imaging of two-pool magnetization transfer model parameters in myelin mutant shaking pup. Neuroimage 62, 1390-1398.
17. Schmierer, K., Tozer, D.J., Scaravilli, F., Altmann, D.R., Barker, G.J., Tofts, P.S., and Miller, D.H. (2007). Quantitative magnetization transfer imaging in postmortem multiple sclerosis brain. J. Magn. Reson. Imaging 26, 41-51.
18. First, M.B., Spitzer, R.L., Gibbon, M. and Williams, J.B. (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. (SCID-I/P). Biometrics Research, New York State Psychiatric Institute: New York.
19. Blake, D.D., Weathers, F.W., Nagy, L.M., Kaloupek, D.G., Gusman, F.D., Charney, D.S., and Keane, T.M. (1995). The development of a Clinician- Administered PTSD Scale. J. Trauma Stress 8, 75-90.
20. Weathers, F.W., Ruscio, A.M., and Keane, T.M. (1999). Psychometric properties of nine scoring rules for the Clinician-Administered Posttraumatic Stress Disorder Scale. Psychol. Assess. 11, 124-133.
21. Killgore, W.D., Cotting, D.I., Thomas, J.L., Cox, A.L., McGurk, D., Vo, A.H., Castro, C.A., and Hoge, C.W. (2008). Post-combat invincibility: Violent combat experiences are associated with increased risk-Taking propensity following deployment. J. Psychiatr. Res. 42, 1112-1121.
22. Forbes, D., Creamer, M., and Biddle, D. (2001). The validity of the PTSD checklist as a measure of symptomatic change in combatrelated PTSD. Behav. Res. Ther. 39, 977-986.
23. Kroenke, K., Spitzer, R.L. and Williams, J.B. (2001). The PHQ-9: Validity of a brief depression severity measure. J. Gen. Intern. Med. 606-613.
24. Buysse, D.J., Reynolds, C.F., 3rd, Monk, T.H., Berman, S.R., and Kupfer, D.J. (1989). The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatry Res. 28, 193-213.
25. Bush, K., Kivlahan, D.R., McDonell, M.B., Fihn, S.D., and Bradley, K.A. (1998). The AUDIT alcohol consumption questions (AUDIT-C): An effective brief screening test for problem drinking. Ambulatory Care Quality Improvement Project (ACQUIP). Alcohol Use Disorders Identification Test. Arch. Intern. Med. 158, 1789-1795.
26. Cicerone, K., and Kalmar, K. (1995). Persistent postconcussion syndrome: The structure of subjective complaints after mild traumatic brain injury. J. Head Trauma Rehabil. 10, 1-17.
27. Stern, R.A., Riley, D.O., Daneshvar, D.H., Nowinski, C.J., Cantu, R.C., and McKee, A.C. (2011). Long-Term consequences of repetitive brain trauma: Chronic traumatic encephalopathy. PM R 3, Suppl 2, S460-S467.
28. Martinez-Martin, P., Gil-Nagel, A., Gracia, L.M., Gomez, J.B., Martinez-Sarries, J., and Bermejo, F. (1994). Unified Parkinson's Disease Rating Scale characteristics and structure. The Cooperative Multicentric Group. Mov. Disord. 9, 76-83.
29. Doty, R.L., Marcus, A., and Lee, W.W. (1996). Development of the 12-item Cross-Cultural Smell Identification Test (CC-SIT). Laryngoscope 106, 353-356.
30. Talairach, J., and Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain. 3-Dimensional Proportional System: An Approach to Cerebral Imaging. Thieme Medical Publishers: New York.
31. Minoshima, S., Berger, K.L., Lee, K.S., and Mintun, M.A. (1992). An automated method for rotational correction and centering of three-dimensional functional brain images. J. Nucl. Med. 33, 1579-1585.
32. Minoshima, S., Frey, K.A., Koeppe, R.A., Foster, N.L., and Kuhl, D.E. (1995). A diagnostic approach in Alzheimer's disease using three-dimensional stereotactic surface projections of fluorine-18-FDG PET. J. Nucl. Med. 36, 1238-1248.
33. Minoshima, S., Koeppe, R.A., Frey, K.A., Ishihara, M., and Kuhl, D.E. (1994). Stereotactic PET atlas of the human brain: Aid for visual interpretation of functional brain images. J. Nucl. Med. 35, 949-954.
34. Minoshima, S., Koeppe, R.A., Frey, K.A., and Kuhl, D.E. (1994). Anatomic standardization: Linear scaling and nonlinear warping of functional brain images. J. Nucl. Med. 35, 1528-1537.
35. Minoshima, S., Koeppe, R.A., Mintun, M.A., Berger, K.L., Taylor, S.F., Frey, K.A., and Kuhl, D.E. (1993). Automated detection of the intercommissural line for stereotactic localization of functional brain images. J. Nucl. Med. 34, 322-329.
36. Yarnykh, V.L. (2010). Optimal radiofrequency and gradient spoiling for improved accuracy of T1 and B1 measurements using fast steadystate techniques. Magn. Reson. Med. 63, 1610-1626.
37. Skinner, T.E., and Glover, G.H. (1997). An extended two-point Dixon algorithm for calculating separate water, fat, and B0 images. Magn. Reson. Med. 37, 628-630.
38. Yarnykh, V.L. (2007). Actual flip-Angle imaging in the pulsed steady state: A method for rapid three-dimensional mapping of the transmitted radiofrequency field. Magn. Reson. Med. 57, 192-200.
39. Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E., Johansen-Berg, H., Bannister, P.R., De Luca, M., Drobnjak, I., Flitney, D.E., Niazy, R.K., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J.M., and Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23, Suppl 1, S208-S219.
40. Liu, X., Zhu, H., Marks, B.L., Katz, L.M., Goodlett, C.B., Gerig, G., and Styner, M. (2009). Voxelwise group analysis of DTI. In: 2009 IEEE International Symposium on Biomedical Imaging (ISBI): From Nano to Macro. Institute of Electrical and Electronics Engineers (IEEE): Boston, MA, pps. 807-810.
41. Hosaka, K., Ishii, K., Sakamoto, S., Sadato, N., Fukuda, H., Kato, T., Sugimura, K., and Senda, M. (2005). Validation of anatomical standardization of FDG PET images of normal brain: Comparison of SPM and NEUROSTAT. Eur. J. Nucl. Med. Mol. Imaging 32, 92-97.
42. Yarnykh, V.L. (2002). Pulsed Z-spectroscopic imaging of cross-relaxation parameters in tissues for human MRI: Theory and clinical applications. Magn. Reson. Med. 47, 929-939.
43. Smith, S.M. (2002). Fast robust automated brain extraction. Hum. Brain Mapp. 17, 143-155.
44. le Gros Clark, W.E. (1936). The termination of ascending tracts in the thalamus of the macaque monkey. J. Anat. 71, 7-40.
45. Worsley, K.J., Evans, A.C., Marrett, S., and Neelin, P. (1992). A three-dimensional statistical analysis for CBF activation studies in human brain. J. Cereb. Blood Flow Metab. 12, 900-918.
46. Adams, J.H., Doyle, D., Ford, I., Gennarelli, T.A., Graham, D.I., and McLellan, D.R. (1989). Diffuse axonal injury in head injury: Definition, diagnosis and grading. Histopathology 15, 49-59.
47. Strich, S.J. (1956). Diffuse degeneration of the cerebral white matter in severe dementia following head injury. J. Neurol. Neurosurg. Psychiatry 19, 163-185.
48. Smith, S.M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T.E., Mackay, C.E., Watkins, K.E., Ciccarelli, O., Cader, M.Z., Matthews, P.M., and Behrens, T.E. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage 31, 1487-1505.
49. Jones, D.K., and Cercignani, M. (2010). Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. 23, 803-820.
50. Edden, R.A., and Jones, D.K. (2011). Spatial and orientational heterogeneity in the statistical sensitivity of skeleton-based analyses of diffusion tensor MR imaging data. J. Neurosci. Methods 201, 213-219.
51. Tustison, N.J., Avants, B.B., Cook, P.A., Kim, J., Whyte, J., Gee, J.C. and Stone, J.R. (2012). Logical circularity in voxel-based analysis: Normalization strategy may induce statistical bias. Hum. Brain Mapp. DOI: 10.1002/hbm.22211. Epub ahead of print
52. Bookstein, F.L. (2001). ''Voxel-based morphometry'' should not be used with imperfectly registered images. Neuroimage 14, 1454-1462.
53. Bookstein, F.L. (1989). Principal warps: Thin-plate splines and the decomposition of deformations. IEEE Trans. Pattern Analysis and Machine Intelligence, 11, 567-585.
54. Ling, G., Bandak, F., Armonda, R., Grant, G., and Ecklund, J. (2009). Explosive blast neurotrauma. J. Neurotrauma 26, 815-825.
55. Maxwell, W.L., Povlishock, J.T., and Graham, D.L. (1997). A mechanistic analysis of nondisruptive axonal injury: A review. J. Neurotrauma 14, 419-440.
56. Kang, X., Herron, T.J., Turken, A.U., and Woods, D.L. (2012). Diffusion properties of cortical and pericortical tissue: Regional variations, reliability and methodological issues. Magn. Reson. Imaging 30, 1111-1122.
57. Hofman, P.A., Verhey, F.R., Wilmink, J.T., Rozendaal, N., and Jolles, J. (2002). Brain lesions in patients visiting a memory clinic with postconcussional sequelae after mild to moderate brain injury. J. Neuropsychiatry Clin. Neurosci. 14, 176-184.
58. Bagley, L.J., McGowan, J.C., Grossman, R.I., Sinson, G., Kotapka, M., Lexa, F.J., Berlin, J.A., and McIntosh, T.K. (2000). Magnetization transfer imaging of traumatic brain injury. J. Magn. Reson. Imaging 11, 1-8.
59. McGowan, J.C., Yang, J.H., Plotkin, R.C., Grossman, R.I., Umile, E.M., Cecil, K.M., and Bagley, L.J. (2000). Magnetization transfer imaging in the detection of injury associated with mild head trauma. AJNR Am. J. Neuroradiol. 21, 875-880.
60. Sinson, G., Bagley, L.J., Cecil, K.M., Torchia, M., McGowan, J.C., Lenkinski, R.E., McIntosh, T.K., and Grossman, R.I. (2001). 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. 22, 143-151.
61. Mamere, A.E., Saraiva, L.A., Matos, A.L., Carneiro, A.A., and Santos, A.C. (2009). Evaluation of delayed neuronal and axonal damage secondary to moderate and severe traumatic brain injury using quantitative MR imaging techniques. AJNR Am. J. Neuroradiol. 30, 947-952.
62. Bergsneider, M., Hovda, D.A., McArthur, D.L., Etchepare, M., Huang, S.C., Sehati, N., Satz, P., Phelps, M.E., and Becker, D.P. (2001). Metabolic recovery following human traumatic brain injury based on FDG-PET: Time course and relationship to neurological disability. J. Head Trauma Rehabil. 16, 135-148.
63. Eibner, C., Schell, T.L., and Jaycox, L.H. (2009). Care of war veterans with mild traumatic brain injury. N. Engl. J. Med. 361, 537.
64. Hoge, C.W., Goldberg, H.M., and Castro, C.A. (2009). Care of war veterans with mild traumatic brain injury-flawed perspectives. N. Engl. J. Med. 360, 1588-1591.
65. Sigford, B., Cifu, D.X. and Vanderploeg, R. (2009). Care of war veterans with mild traumatic brain injury. N. Engl. J. Med. 361, 536.
66. Ayling, E., Aghajani, M., Fouche, J.P., and van der Wee, N. (2012). Diffusion tensor imaging in anxiety disorders. Curr. Psychiatry Rep. 197-202.
67. Broglio, S.P., Eckner, J.T., Surma, T., and Kutcher, J.S. (2011). Postconcussion cognitive declines and symptomatology are not related to concussion biomechanics in high school football players. J. Neurotrauma 28, 2061-2068.
68. Minoshima, S., Foster, N.L., Petrie, E.C., Albin, R.L., Frey, K.A., and Kuhl, D.E. (2002). Neuroimaging in dementia with Lewy bodies: Metabolism, neurochemistry, and morphology. J. Geriatr. Psychiatry Neurol. 15, 200-209.
69. Minoshima, S., Sasaki, T., and Petrie, E. (2009). FDG PET imaging of dementia: Principles and clinical applications, in: Principles and Practice of PET and PET/CT. R.L. Wahl (ed). Lippincott, Williams & Wilkins: Philadelphia, pps. 500-515.
70. Chappell, M.H., Ulug, A.M., Zhang, L., Heitger, M.H., Jordan, B.D., Zimmerman, R.D., and Watts, R. (2006). Distribution of microstructural damage in the brains of professional boxers: A diffusion MRI study. J. Magn. Reson. Imaging 24, 537-542.
71. Oishi, K., Andreia, F., van Zijl, P.C., Mori, S. (2011). mRI Atlas of Human White Matter 2nd ed. London, Academic Press.