Advanced neuroimaging to quantify myelin in vivo: Application to mild TBI

References

• Roebuck-Spencer T, Sherer M. Moderate and severe traumatic brain injury. In: Morgan JE, Ricker JH, editors. Textbook of Clinical Neuropsychology. New York: Taylor and Francis; 2008. p 411–429.
   Google Scholar
• Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet 1974;304:81–84.
   Google Scholar
• VA/DoD. VA/DOD clinical practice guideline for management of concussion/mild traumatic brain injury. Washington, DC: Va/DoD; 2009.
   Google Scholar
• Delano-Wood L, Bangen KJ, Sorg SF, Clark AL, Schiehser DM, Luc N, Bondi MW, 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 and Behavior 2015;9:1–13.
   PubMed Web of Science ®Google Scholar
• Niogi SN, Mukherjee P, Ghajar J, Johnson C, Kolster RA, Sarkar R, Lee H, Meeker M, Zimmerman RD, Manley GT, et al. Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. American Journal of Neuroradiology 2008;29:967–973.
   PubMed Web of Science ®Google Scholar
• Gale SD, Johnson SC, Bigler ED, Blatter DD. Nonspecific white matter degeneration following traumatic brain injury. Journal of the International Neuropsychological Society 1995;1:17–28.
   PubMedGoogle Scholar
• Bigler ED, Maxwell WL. Neuropathology of mild traumatic brain injury: relationship to neuroimaging findings. Brain Imaging and Behavior 2012;6:108–136.
   PubMed Web of Science ®Google Scholar
• Bramlett HM, Kraydieh S, Green EJ, Dietrich D. Temporal and regional patterns of axonal damage following traumatic brain injury: a beta-amyloid precursor protein immunocytochemical study in rats. Journal of Neuropathology & Experimental Neurology 1997;56:1132–1141.
   PubMed Web of Science ®Google Scholar
• Miles L, Grossman RI, Johnson G, Babb JS, Diller E, Inglese M. Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Injury 2008;22:115–122.
   PubMed Web of Science ®Google Scholar
• Shenton M, Hamoda HM, Schneiderman JS, Bouix S, Pasternak Y, Rathi Y, Vu MA, Purohit MP, Helmer K, Koerte I, et al. A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging and Behavior 2012;6:137–192.
   PubMed Web of Science ®Google Scholar
• Yuh EL, Cooper SR, Mukherjee P, Yue JK, Lingsma HF, Gordon WA, Valadka AB, Okonkwo DO, Schnyer DM, Vassar MJ, et al. Diffusion tensor imaging for outcome prediction in mild traumatic brain injury: a TRACK-TBI study. Journal of Neurotrauma 2014;31:1457–1477.
   PubMed Web of Science ®Google Scholar
• Mierzwa AJ, Marion CM, Sullivan GM, McDaniel DP, Armstrong RC. Components of myelin damage and repair in the progression of white matter pathology after mild traumatic brain injury. Journal of Neuropathology and Experimental Neurology 2015;74:218–232.
   PubMed Web of Science ®Google Scholar
• Maxwell WL, Domleo A, McColl G, Saeed SJ, Graham DI. Post-acute alterations in the axonal cytoskeleton after traumatic axonal injury. Journal of Neurotrauma 2003;20:151–168.
   PubMed Web of Science ®Google Scholar
• Maxwell WL, Kosanlavit R, McCreath BJ, Reid O, Graham DI. Freeze-fracture and cytochemical evidence for structural and functional alteration in the axolemma and myelin sheath of adult guinea pig optic nerve fibers after stretch injury. Journal of Neurotrauma 1999;16:273–284.
   PubMed Web of Science ®Google Scholar
• Rubovitch V, Ten-Bosch M, Zohar O, Harrison CR, Tempel-Brami C, Stein E, Hoffer BJ, Balaban CD, Schreiber S, Chiu W-T, et al. A mouse model of blast-induced mild traumatic brain injury. Experimental Neurology 2011;232:280–289.
   PubMed Web of Science ®Google Scholar
• Bramlett HM, Dietrich DW. Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathologica 2002;103:607–614.
   PubMed Web of Science ®Google Scholar
• Donovan V, Kim C, Anugerah AK, Coats JS, Udochuwku O, Pardo AC, Obenaus A. Repeated mild traumatic brain injury results in long-term white-matter disruption. Journal of Cerebral Blood Flow & Metabolism 2014;34:715–723.
   PubMed Web of Science ®Google Scholar
• Shi H, Hu X, Leak RK, Shi Y, An C, Suenaga J, Chen J, Gao Y. Demyelination as a rational therapeutic target for ischemic or traumatic brain injury. Experimental Neurology 2015;272:17–25.
   PubMed Web of Science ®Google Scholar
• Tsunoda I, Fujinami RS. Inside-out versus outside-in models for virus induced demyelination: axonal damage triggering demyelination. Springer Seminars in Immunopathology 2002;24;105–125.
   Google Scholar
• Grin’kina, NM, Abdel-Baki SG, Berghold P. Reversible behavioral deficits in rats during a cycle of demyelination-remyelination of the fimbria. PloS ONE 2013;8:e53775.
   Google Scholar
• Crawford MA, Knight RG, Alsop BL. Speed of word retrieval in postconcussion syndrome. Journal of the International Neuropsychological Society 2007;13:178–182.
   PubMed Web of Science ®Google Scholar
• Demery JA, Larson MJ, Dixit NK, Bauer RM, Perlstein WM. Operating characteristics of executive functioning tests following traumatic brain injury. The Clinical Neuropsychologist 2010;24:1292–1308.
   PubMed Web of Science ®Google Scholar
• McCrea M. Mild traumatic brain injury and postconcussion syndrome. New York: Oxford University Press; 2008.
   Google Scholar
• Bombardier CH, Hoekstra T, Dikmen S, Fann JR. Depression trajectories during the first year after traumatic brain injury. Journal of Neurotrauma 2016; online ahead of print.
   PubMedGoogle Scholar
• Taylor BC, Hagel EM, Carlson KF, Cifu DX, Cutting A, Bidelspach DE, Sayer NA. Prevalence and costs of co-occurring traumatic brain injury with and without psychiatric disturbance and pain among Afghanistan and Iraq War Veteran VA users. Medical Care 2012;50:342–346.
   PubMed Web of Science ®Google Scholar
• Bigler ED, Maxwell WL. Neuroimaging and neuropathology of TBI. NeuroRehabilitation 2011;28:63–74.
   PubMed Web of Science ®Google Scholar
• Hulkower MB, Poliak DB, Rosenbaum SB, Zimmerman ME, Lipton ML. A decade of DTI in traumatic brain injury: 10 years and 100 articles later. American Journal of Neuroradiology 2013;34:2064–2074.
   PubMed Web of Science ®Google Scholar
• Johansen-Berg H, Behrens TE, editors. Diffusion MRI: from quantitative measurement to in vivo neuroanatomy. London, UK: Academic Press; 2013.
   Google Scholar
• Armstrong RC, Mierzwa AJ, Marion CM, Sullivan GM. White matter involvement after TBI: clues to axon and myelin repair capacity. Experimental Neurology 2016;275:328–333.
   PubMed Web of Science ®Google Scholar
• Raine CS. Morphology of myelin and myelination. In Morell P, editor. Myelin. New York (NY): Springer-Verlag; 1984. p 1–50.
   Google Scholar
• Norton WT, Cammer W. Isolation and characterization of myelin. In Morell P, editor. Myelin. New York (NY): Springer-Verlag; 1984. p 147–195.
   Google Scholar
• Ludwin S. The perineuronal satellite oligodendrocyte. Acta Neuropathologica 1979;47:49–53.
   PubMed Web of Science ®Google Scholar
• Irvine K, Blakemore W. Remyelination protects axons from demyelination-associated axon degeneration. Brain 2008;131:1464–1477.
   PubMed Web of Science ®Google Scholar
• Sánchez I, Hassinger L, Paskevich PA, Shine HD, Nixon RA. Oligodendroglia regulate the regional expansion of axon caliber and local accumulation of neurofilaments during development independently of myelin formation. The Journal of Neuroscience 1996;16:5095–5105.
   PubMed Web of Science ®Google Scholar
• Uschkureit T, Spörkel O, Stracke J, Büssow H, Stoffel W. Early onset of axonal degeneration in double (plp−/− mag−/−) and hypomyelinosis in triple (plp−/− mbp−/− mag−/−) mutant mice. The Journal of Neuroscience 2000;20:5225–5233.
   PubMed Web of Science ®Google Scholar
• McTigue DM, Tripathi RB. The life, death, and replacement of oligodendrocytes in the adult CNS. Journal of Neurochemistry 2008;107:1–19.
   PubMed Web of Science ®Google Scholar
• Lotocki G, de Rivero Vaccari J, Alonso O, Molano JS, Nixon R, Safavi P, Dietrich WD, Bramlett HM. Oligodendrocyte vulnerability following traumatic brain injury in rats. Neuroscience Letters 2011;499:143–148.
   PubMed Web of Science ®Google Scholar
• Flygt J, Djupsjö A, Lenne F, Marklund N. Myelin loss and oligodendrocyte pathology in white matter tracts following traumatic brain injury in the rat. European Journal of Neuroscience 2013;38:2153–2165.
   PubMed Web of Science ®Google Scholar
• Johnson VE, Stewart W, Smith DH. Axonal pathology in traumatic brain injury. Experimental Neurology 2013;246:35–43.
   PubMed Web of Science ®Google Scholar
• Kinnunen KM, Greenwood R, Powell JH, Leech R, Hawkins PC, Bonnelle V, Patel MC, Counsell SJ, Sharp DJ. White matter damage and cognitive impairment after traumatic brain injury. Brain 2011;134:449–463.
   PubMed Web of Science ®Google Scholar
• Sharp DJ, Beckmann CF, Greenwood R, Kinnunen KM, Bonnelle V, De Boissezon X, Powell JH, Counsell SJ, Patel MC, Leech R. Default mode network functional and structural connectivity after traumatic brain injury. Brain 2011;134:2233–2247.
   PubMed Web of Science ®Google Scholar
• Büki A, Povlishock JT. All roads lead to disconnection?–Traumatic axonal injury revisited. Acta Neurochirurgica 2006;148:181–194.
   PubMed Web of Science ®Google Scholar
• Conti AC, Raghupathi R, Trojanowski JQ, McIntosh TK. Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. The Journal of Neuroscience 1998;18:5663–5672.
   PubMed Web of Science ®Google Scholar
• Raghupathi R, Conti AC, Graham DI, Krajewski S, Reed JC, Grady MS, Trojanowski JQ, McIntosh TK. Mild traumatic brain injury induces apoptotic cell death in the cortex that is preceded by decreases in cellular Bcl-2 immunoreactivity. Neuroscience 2002;110:605–616.
   PubMed Web of Science ®Google Scholar
• Liu MC, Akle V, Zheng W, Kitlen J, O’Steen B, Larner SF, Dave JR, Tortella FC, Hayes RL, Wang KK. Extensive degradation of myelin basic protein isoforms by calpain following traumatic brain injury. Journal of Neurochemistry 2006;98:700–712.
   PubMed Web of Science ®Google Scholar
• Stys PK. Anoxic and ischemic injury of myelinated axons in CNS white matter: from mechanistic concepts to therapeutics. Journal of Cerebral Blood Flow & Metabolism 1998;18:2–5.
   PubMed Web of Science ®Google Scholar
• Sullivan GM, Mierzwa AJ, Kijpaisalratana N, Tang H, Wang Y, Song SK, Selwyn R, Armstrong RC. Oligodendrocyte lineage and subventricular zone response to traumatic axonal injury in the corpus callosum. Journal of Neuropathology & Experimental Neurology 2013;72:1106–1125.
   PubMed Web of Science ®Google Scholar
• Fields RD. White matter in learning, cognition and psychiatric disorders. Trends in Neurosciences 2008;31:361–370.
   PubMed Web of Science ®Google Scholar
• Shaw K, MacKinnon MA, Raghupathi R, Saatman KE, McLntosh TK, Graham DI. TUNEL-positive staining in white and grey matter after fatal head injury in man. Clinical Neuropathology 2000;20:106–112.
   Web of Science ®Google Scholar
• Ng HR, Mahaliyana R, Poon W. The pathological spectrum of diffuse axonal injury in blunt head trauma: assessment with axon and myelin stains. Clinical Neurology and Neurosurgery 1994;96:24–31.
   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
• Bruce CC, Zhao C, Franklin RJ. Remyelination—an effective means of neuroprotection. Hormones and Behavior 2010;57:56–62.
   PubMed Web of Science ®Google Scholar
• Armstrong RC, Mierzwa AJ, Sullivan GM, Sanchez MA. Myelin and oligodendrocyte lineage cells in white matter pathology and plasticity after traumatic brain injury. Neuropharmacology 2015; online ahead of print.
   Google Scholar
• Dams-O’Connor K, Spielman L, Singh A, Gordon WA, Lingsma HF, Maas AI, Manley GT, Mukherjee P, Okonkwo DO, Puccio AM, Schnyer DM. The impact of previous traumatic brain injury on health and functioning: A TRACK-TBI study. Journal of Neurotrauma 2013;30:2014–2020.
   PubMed Web of Science ®Google Scholar
• Donders J, Strong CA. Clinical utility of the Wechsler Adult Intelligence Scale–Fourth Edition after traumatic brain injury. Assessment 2014;22:17–22.
   PubMed Web of Science ®Google Scholar
• McKee AC, Robinson ME. Military-related traumatic brain injury and neurodegeneration. Alzheimer’ & Dementia 2014;10:S242–S253.
   PubMed Web of Science ®Google Scholar
• Bazarian JJ, Zhong J, Blyth B, Zhu T, Kavcic V, Peterson D. Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. Journal of Neurotrauma 2007;24:1447–1459.
   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;42:503–514.
   PubMed Web of Science ®Google Scholar
• Huisman TA, Schwamm LH, Schaefer PW, Koroshetz WJ, Shetty-Alva N, Ozsunar Y, Wu O, Sorensen AG. Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. American Journal of Neuroradiology 2004;25:370–376.
   PubMed Web of Science ®Google Scholar
• Inglese M, Makani S, Johnson G, Cohen BA, Silver JA, Gonen O, Grossman RI. Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. Journal of Neurosurgery 2005;103:298–303.
   PubMed Web of Science ®Google Scholar
• Kraus MF, Susmaras T, Caughlin BP, Walker CJ, Sweeney JA, Little DM. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 2007;130:2508–2519.
   PubMed Web of Science ®Google Scholar
• Levin HS, Wilde E, Troyanskaya M, Petersen NJ, Scheibel R, Newsome M, Radaideh M, Wu T, Yallampalli R, Chu Z, Li X. Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. Journal of Neurotrauma 2010;27:683–694.
   PubMed Web of Science ®Google Scholar
• Bazarian JJ, Donnelly K, Peterson DR, Warner GC, Zhu T, Zhong J. The relation between posttraumatic stress disorder and mild traumatic brain injury acquired during Operations Enduring Freedom and Iraqi Freedom. The Journal of Head Trauma Rehabilitation 2013;28:1–2.
   PubMed Web of Science ®Google Scholar
• Matthews SC, Strigo IA, Simmons AN, O’Connell RM, Reinhardt LE, Moseley SA. A multimodal imaging study in US veterans of Operations Iraqi and Enduring Freedom with and without major depression after blast-related concussion. Neuroimage 2011;54:S69–S75.
   PubMed Web of Science ®Google Scholar
• Choi KS, Holtzheimer PE, Franco AR, et al. Reconciling variable findings of white matter integrity in major depressive disorder. Neuropsycholopharmacology 2014;39:1332–1339.
   PubMed Web of Science ®Google Scholar
• Spader HS, Ellermeier A, O’Muircheartaigh J, Dean III DC, Dirks H, Boxerman JL, Cosgrove GR, Deoni SC. Advances in myelin imaging with potential clinical application to pediatric imaging. Neurosurgical Focus 2013;34:E9.
   Google Scholar
• Thomalla G, Glauche V, Koch MA, Beaulieu C, Weiller C, Röther J. Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. Neuroimage 2004;22:1767–1774.
   PubMed Web of Science ®Google Scholar
• 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;20:1714–1722.
   PubMed Web of Science ®Google Scholar
• Kumar R, Gupta RK, Husain M, Chaudhry C, Srivastava A, Saksena S, Rathore RK. Comparative evaluation of corpus callosum DTI metrics in acute mild and moderate traumatic brain injury: its correlation with neuropsychometric tests. Brain Injury 2009;23:675–685.
   PubMed Web of Science ®Google Scholar
• Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips JP, Doezema D, Reichard R, Yeo RA. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 2010;74:643–650.
   PubMed Web of Science ®Google Scholar
• Klawiter EC, Schmidt RE, Trinkaus K, Liang HF, Budde MD, Naismith RT, Song SK, Cross AH, Benzinger TL. Radial diffusivity predicts demyelination in ex vivo multiple sclerosis spinal cords. Neuroimage 2011;55:1454–1460.
   PubMed Web of Science ®Google Scholar
• Madden DJ, Bennett IJ, Song AW. Cerebral white matter integrity and cognitive aging: contributions from diffusion tensor imaging. Neuropsychology Review 2009;19:415–435.
   PubMed Web of Science ®Google Scholar
• Wheeler-Kingshott CA, Cercignani M. About ‘axial’ and ‘radial’ diffusivities. Magnetic Resonance in Medicine 2009;61:1255–1260.
   PubMed Web of Science ®Google Scholar
• Whittall KP, Mackay AL, Graeb DA, Nugent RA, Li DK, Paty DW. In vivo measurement of T2 distributions and water contents in normal human brain. Magnetic Resonance in Medicine 1997;37:34–43.
   PubMed Web of Science ®Google Scholar
• Mädler B, Drabycz SA, Kolind SH, Whittall KP, MacKay AL. Is diffusion anisotropy an accurate monitor of myelination?: Correlation of multicomponent T2 relaxation and diffusion tensor anisotropy in human brain. Magnetic Resonance Imaging 2008;26:874–888.
   PubMed Web of Science ®Google Scholar
• Laule C, Leung E, Li DK, Traboulsee AL, Paty DW, MacKay AL, Moore GR. Myelin water imaging in multiple sclerosis: quantitative correlations with histopathology. Multiple Sclerosis 2006;12:747–753.
   PubMed Web of Science ®Google Scholar
• Stanisz GJ, Webb S, Munro CA, Pun T, Midha R. MR properties of excised neural tissue following experimentally induced inflammation. Magnetic Resonance in Medicine 2004;51:473–479.
   PubMed Web of Science ®Google Scholar
• Webb S, Munro CA, Midha R, Stanisz GJ. Is multicomponent T2 a good measure of myelin content in peripheral nerve?. Magnetic Resonance in Medicine 2003;49:638–645.
   PubMed Web of Science ®Google Scholar
• Deoni SC. Correction of main and transmit magnetic field (B0 and B1) inhomogeneity effects in a multicomponent-driven equilibrium single-pule observation of T1 and T2. Magnetic Resonance Medicine 2011;65:1021–1035.
   PubMed Web of Science ®Google Scholar
• Deoni SC, Rutt BK, Arun T, Pierpaoli C, Jones DK. Gleaning multicomponent T1 and T2 information from steady-state imaging data. Magnetic Resonance in Medicine 2008;60:1372–1387.
   PubMed Web of Science ®Google Scholar
• Kolind S, Matthews L, Johansen-Berg H, Leite MI, Williams SC, Deoni S, Palace J. Myelin water imaging reflects clinical variability in multiple sclerosis. Neuroimage 2012;60:263–270.
   PubMed Web of Science ®Google Scholar
• Kolind S, Seddigh A, Combes A, Russell-Schulz B, Tam R, Yogendrakumar V, Deoni S, Sibtain NA, Traboulsee A, Williams SC, Barker GJ. Brain and cord myelin water imaging: a progressive multiple sclerosis biomarker. NeuroImage: Clinical 2015;9:574–580.
   PubMed Web of Science ®Google Scholar
• O’Muircheartaigh J, Dean DC, Ginestet CE, Walker L, Waskiewicz N, Lehman K, Dirks H, Piryatinsky I, Deoni SC. White matter development and early cognition in babies and toddlers. Human Brain Mapping 2014;35:4475–4487.
   PubMed Web of Science ®Google Scholar
• Chevalier N, Kurth S, Doucette MR, Wiseheart M, Deoni SC, Dean III DC, O’Muircheartaigh J, Blackwell KA, Munakata Y, LeBourgeois MK. Myelination is associated with processing speed in early childhood: Preliminary insights. PloS one 2015;10:e0139897.
   Google Scholar
• Dean DC, Jerskey BA, Chen K, Protas H, Thiyyagura P, Roontiva A, O’Muircheartaigh J, Dirks H, Waskiewicz N, Lehman K, Siniard AL. Brain differences in infants at differential genetic risk for late-onset Alzheimer disease: a cross-sectional imaging study. JAMA Neurology 2014;71:11–22.
   PubMed Web of Science ®Google Scholar
• Lamar M, Zhou XJ, Charlton RA, Dean D, Little D, Deoni SC. In vivo quantification of white matter microstructure for use in aging: a focus on two emerging techniques. The American Journal of Geriatric Psychiatry 2014;22:111–121.
   PubMed Web of Science ®Google Scholar
• Wright AD, Jarrett M, Vavasour I, Shahinfard E, Kolind S, van Donkelaar P, Taunton J, Li D, Rauscher A. Myelin water fraction is transiently reduced after a single mild traumatic brain injury–A prospective cohort study in collegiate hockey players. PloS one 2016;11:e0150215.
   PubMed Web of Science ®Google Scholar
• Deoni SC, Kolind SH. Investigating the stability of mcDESPOT myelin water fraction values derived using a stochastic region contraction approach. Magnetic Resonance in Medicine 2015;73:161–169.
   PubMed Web of Science ®Google Scholar