Traumatic brain injury in the neonate, child and adolescent human: An overview of pathology

International Journal of Developmental Neuroscience

Volumn 30, Issue 3, 2012, Pages 167-183

  Maxwell, William L ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Hematoma; Immature or unmyelinated axons; Inflammatory response; Macrophages and microglia; Myelination; Neuronal injury; Oligodendrocytes; TBI; The neurovascular unit

Indexed keywords

ADOLESCENCE; ADOLESCENT; ADULTHOOD; ARTICLE; BIRTH; BRAIN DEVELOPMENT; BRAIN GROWTH; CELL INTERACTION; CENTRAL NERVOUS SYSTEM; CHILD; CHILDHOOD; HUMAN; INFANCY; LONG TERM CARE; NERVE CELL; NERVE CELL LESION; NEUROIMAGING; NEWBORN; NON INVASIVE MEASUREMENT; NONHUMAN; PATHOPHYSIOLOGY; PATIENT CARE; PRIORITY JOURNAL; TRAUMATIC BRAIN INJURY;

ADOLESCENT; AGING; BRAIN; BRAIN INJURIES; CHILD; CHILD, PRESCHOOL; HUMANS; INFANT; INFANT, NEWBORN;

EID: 84859422762     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2011.12.008     Document Type: Article

References (129)

1. Adams J.H., Doyle D., Ford I., Gennarelli T.A., Graham D.I., McLellan D.R. Diffuse axonal head injury: definition, diagnosis and grading. Histopathology 1989, 1:49-59.
2. Ahmed S.M., Rzigalinski B.A., Willoughby K.A., Sitterding H.A., Ellis E.F. Stretch-induced injury alters mitochondrial membrane potential and cellular ATP in cultured astrocytes and neurons. J. Neurochem. 2000, 74:1951-1960.
3. Anderson V., Spencer-Smith M., Leventer R., Coleman L., Anderson P., Williams J., Greenham M., Jacobs M. Childhood brain insult: can age at insult help us predict outcome?. Brain 2009, 132:45-56.
4. Anderson V., Spencer-Smith M., Wood A. Do children really recover better? Neurobehavioral plasticity after early brain insult. Brain 2011, 10.1093/brain/awr103.
5. Asato M.R., Terwilliger R., Woo J., Luna B. White matter development in adolescence: a DTI study. Cereb. Cortex 2010, 20:2122-2131.
6. Ball G., Boardman J.P., Rueckert D., Aljabar P., Arichi T., Merchant N., Gousias I.S., Edwards A.D., Counsell S.J. The effect of preterm birth on thalamic and cortical development. Cereb. Cortex 2011, 10.1093/cercor/bhr176.
7. Ballesteros M.C., Hansen P.E., Soila K. MR imaging of the developing human brain part 2. Postnatal development. RadioGraphics 1993, 13:611-622.
8. Barlow K.M., Thomson E., Johnson D., Minns R.A. Late neurologic and cognitive sequelae of inflicted traumatic brain injury in infancy. Pediatrics 2005, 116:e174-e185.
9. Barnea-Goraly N., Menon V., Eckert M., Tamm L., Bammer R., Karchemskiy Dant C.C., Reiss L. White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb. Cortex 2005, 15:1848-1854.
10. Barrientos S.A., Martinez N.W., Yoo S., Jara J.S., Zamorano S., Hetz C., Twiss J.L., Alvarez J., Court F.A. Axonal degeneration is mediated by the mitochondrial permeability transition pore. J. Neurosci. 2011, 31:966-978.
11. Beirowski B., Adalbert R., Wagner D., Grumme D.S., Addicks K., Ribchester R.R., Coleman M.P. The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci. 2005, 6. 10.1186/1471-2202-6-6.
12. Bell J.E., Becher J.-C., Wyatt B., Keeling J.W., McIntosh N. Brain damage and axonal injury in a Scottish cohort of neonatal deaths. Brain 2005, 128:1070-1081.
13. Berkelaar M., Clarke D.B., Wang Y.C., Bray G.M., Aguayo A.J. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J. Neurosci. 1994, 14:4368-4374.
14. Bigler E.D., Maxwell W.L. Neuroimaging and neuropathology of TBI. NeuroRehab 2011, 28:1-12.
15. Bittigau P., Sifringer M., Felderhoff-Mueser U., Hansen H.H., Ikonomidou C. Neuropathological and biochemical features of traumatic injury in the developing brain. Neurotox. Res. 2003, 5:475-490.
16. Blakemore S-J. The social brain in adolescence. Nat. Rev. Neurosci. 2009, 9:267-277.
17. Bonnier C., Marique P., Van Hout A., Potelle D. Neurodevelopmental outcome after severe traumatic brain injury in very young children: role for subcortical lesions. J. Child Neurol. 2007, 22:519-529.
18. 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 2011, 134:2248-2260.
19. Büki A., Siman R., Trojanowski J.Q., Povlishock J.T. The role of calpain-mediated spectrin proteolysis in traumatically induced axonal injury. J. Neuropathol. Exp. Neurol. 1999, 58:365-375.
20. Büki, A., Okonkwo, D.O., Wang, K.K.W., Povlishock J.T. 2000. Cytochrome c release and caspase activation in traumatic axonal injury. J. Neurosci. 20, 2825-2834.
21. 11C] (R)-PK11195-PET following herpes encephalitis reveals projected neuronal damage beyond the primary focal lesion. Brain 2001, 124:2014-2027.
22. Case M.E. Abusive head injuries in infants and young children. Legal Med. 2007, 9:83-87.
23. Case M.E. Inflicted traumatic brain injury in infants and young children. Brain Pathol. 2008, 18:571-582.
24. Case M.E. Accidental traumatic head injury in infants and young children. Brain Pathol. 2008, 18:583-589.
25. Christian C.W., Block R. Abusive head trauma in infants and children. Pediatrics 2009, 123:1409-1411.
26. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
27. Ding X.-Q., Sun Y., Braaß H., Illies T., Zeumer H., Lanfermann H., Fiehler J. Evidence of rapid ongoing brain development beyond 2 years of age detected by fiber tracking. Am. J. Neuroradiol. 2008, 29:1261-1265.
28. Dobbing J., Sands J. Quantitative growth and development of human brain. Arch. Dis. Child 1973, 48:757-767.
29. Dratviman-Storobinsky O., Hasanreisoglu M., Offen D., Barhum Y., Weinberger D., Goldenberg-Cohen N. Progressive damage along the optic nerve following induction of crush injury or rodent anterior ischemic optic neuropathy in transgenic mice. Mol. Vision 2008, 14:2171-2179.
30. Duhaime A.C., Gennarelli T.A., Thibault L.E., Bruce D.A., Margulies S.S., Wiser R. The shaken baby syndrome. A clinical, pathological, and biomechanical study. J. Neurosurg. 1987, 66:409-415.
31. Duhaime A.C., Alario A.J., Lewander W.J., Schut L., Sutton L.N., Seidl T.S., et al. Head injury in very young children: mechanisms, injury types, and ophthalmologic findings in 100 hospitalized children younger than 2 years of age. Pediatrics 1992, 90:179-185.
32. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35:495-516.
33. Emery B. Regulation of oligodendrocytes differentiation and myelination. Science 2010, 330:779-782.
34. Ewing-Cobbs L., Prasad M.R., Landry S.H., Kramer L., DeLeon R. Executive functions following traumatic brain injury in young children: a preliminary analysis. Dev. Neuropsychol. 2004, 26:487-512.
35. Ewing-Cobbs L., Prasad M.R., Swank P., et al. Arrested development and disrupted callosal microstructure following pediatric traumatic brain injury: relation to neurobehavioral outcomes. Neuroimage 2008, 42:1305-1315.
36. Fitzgerald M., Bartlett C.A., Harvey A.R., Dunlop S.A. Early events of secondary degeneration after partial optic nerve transection: an immunohistochemical study. J. Neurotrauma 2010, 27:439-452.
37. Geddes J.F., Vowles G.H., Beer T.W., Ellison D.W. The diagnosis of diffuse axonal injury: implications for forensic practice. Neuropathol. Appl. Neurobiol. 1997, 23:339-374.
38. Geddes J.F., Whitwell H.L., Graham D.I. Traumatic axonal injury: practical issue for diagnosis in medicolegal cases. Neuropathol. Appl. Neurobiol. 2000, 26:105-116.
39. Geddes J.F., Hackshaw A.K., Vowles G.H., Nickols C.D., Whitwell H.L. Neuropathology of inflicted head injury in children I. Patterns of brain damage. Brain 2001, 124:1290-1298.
40. Geddes J.F., Vowles G.H., Hackshaw A.K., Nickols C.D., Scott I.S., Whitwell H.L. Neuropathology of inflicted head injury in children II. Microscopic brain injury in infants. Brain 2001, 124:1299-1306.
41. Gerlach R., Dittrich S., Schneider W., Ackermann H., Seifert V., Kieslich M. Traumatic epidural hematomas in children and adolescents: Outcome analysis in 39 consecutive unselected cases. Pediatr. Emerg. Care 2009, 25:164-169.
42. Giedd J.N. Structural magnetic resonance imaging of the adolescent brain. Ann. N. Y. Acad. Sci. 2004, 1021:77-85.
43. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2:861-863.
44. Gilmore J.H., Lin W., Prastawa M.W., Looney C.B., Vetsa Y.S.K., Knickmeyer R.C., Evans D.D., Smith J.K., Hamer R.M., Lieberman J.A., Gerig G. Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J. Neurosci. 2007, 27:1255-1260.
45. Giza C.C. Lasting effects of pediatric traumatic brain injury. Indian J. Neurotrauma 2006, 3:19-26.
46. Gorrie C., Duflou J., Brown J., Gibson T., Waite P.M.E. Extent and distribution of vascular injury in pediatric road fatalities. J. Neurotrauma 2001, 18:849-860.
47. Gorrie C., Oakes S., Duflou J., Blumbergs P., Waite P.M.E. Axonal injury in children after motor vehicle crashes: extent, distribution, and size of axonal swellings using β-APP immunohistochemistry. J. Neurotrauma 2002, 19:1171-1192.
48. Graham D.I., Adams J.H., Doyle D. Ischaemic brain damage in fatal non-missile head injuries. J. Neurol. Sci. 1978, 39(2-3):213-234.
49. Graham D.I., Ford I., Adams J.H., Doyle D., Lawrence A.E., McLellan D.R., Ng H.K. Fatal head injury in children. J. Clin. Pathol. 1989, 42:18-22.
50. Groeschel S., Vollmer B., King M.D., Connelly A. Developmental changes in cerebral grey and white matter volume from infancy to adulthood. Int. J. Devl. Neurosci. 2010, 28:481-489.
51. Hagmann P., Sporns O., Madan N., Cammoun L., Pienaar R., Wedeen V.J., Meuli R., Thiran J.-P., Grant P.E. White matter maturation reshapes structural connectivity in the late developing human brain. Proc. Nat. Acad. Sci. U. S. A. 2010, 107:19067-109072.
52. Hafiz M., Saffari M. Characteristic differences in neuroimaging and physical findings between non-accidental and accidental traumatic brain injury in young children. A local experience in general hospital of Kuala Lumpur. Med. J. Malaysia 2011, 66:95-100.
53. Hamilton N., Vayro S., Kirchhoff F., Verkhratsky A., Robbins J., Gorecki D.C., Butt A.M. Mechanisms of ATP and glutamate-mediated calcium signaling in white matter astrocytes. Glia 2008, 56:734-749.
54. Hausmann R., Biermann T., Wiest I., Tubel J., Betz P. Neuronal apoptosis following human brain injury. Int. J. Legal Med. 2004, 118:32-36.
55. Hobbs C., Childs A-M., Wynne J., Livingston J., Seal A. Subdural haematoma and effusion in infancy: an epidemiological study. Arch. Dis. Child 2005, 90:952-955.
56. Horneman G., Emanuelson I. Cognitive outcome in children and young adults who sustained severe and moderate traumatic brain injury 10 years earlier. Brain Injury 2009, 23(11):907-914.
57. Huang H., Zhang J., Wakana S., Zhang W., Ren T., Richards L.J., Yarowsky P., Donohue P., Graham E., van Zijl P.C.M., Mori S. White and gray matter development in human fetal, newborn and pediatric brains. NeuroImage 2006, 33:27-38.
58. Inglese M., Bomsztyk E., Gonen O., Mannon L.J., Grossman R.I., Rusinek H. Dilated perivascular spaces: hallmarks of mild traumatic brain injury. AJNR 2005, 26:719-724.
59. Iwata S., Bainbridge A., Nakamura T., Tamura M., Takashima S., Matsuishi T., Iwata O. Subtle white matter injury is common in term-born infants with a wide range of risks. Int. J. Devel. Neurosci. 2010, 28:573-580.
60. Jafari S.S., Maxwell W.L., Neilson M., Graham D.I. Axonal cytoskeletal changes after non-disruptive axonal injury. J. Neurocytol. 1997, 26:207-221.
61. Jafari S.S., Neilson M., Graham D.I., Maxwell W.L. Axonal cytoskeletal changes after non-disruptive axonal injury. II Intermediate sized axons. J. Neurotrauma 1998, 15:955-966.
62. Jakovceski I., Zecevic N. Sequence of oligodendrocytes development in the human fetal telecephalon. Glia 2005, 49:480-491.
63. Jakovceski I., Filipovic R., Mo Z., Rakic S., Zecevic N. Oligodendrocyte development and the onset of myelination in the human fetal brain. Front. Neuroanat. 2009, 3:1-15.
64. Jette N., Coderre E., Nikolaeva M.A., Enright P.D., Iwata A., Smith D.H., Jiang Q., Stys P.K. Spatiotemporal distribution of spectrin breakdown products induced by anoxia in adult rat optic nerve in vitro. J. Cereb. Blood Flow Metab. 2006, 26:777-786.
65. Johnson M.W., Stoll L., Rubio A., Troncoso J., Pletnikova O., Fowler D.R., Li L. Axonal injury in young pediatric head trauma: A comparison study of β-amyloid precursor protein (β-APP) immunohistochemical staining in traumatic and nontraumatic deaths. J. Forensc. Sci. 2011, 56:1198-1205.
66. Kennard M. Relation of age to motor impairment in man and in subhuman primates. Arch. Neurol. Psychiatr. 1940, 44:377-397.
67. Koehler R.C., Gebremedhin D., Harder D.R. Role of astrocytes in cerebrovascular regulation. J. Appl. Physiol. 2006, 100:307-317.
68. Kinnunen K.M., Greenwood R., Powell J.H., Leech R., Hawkins P.C., Bonnelle V., Patel M.C., Counsell S.J., Sharp D.J. White matter damage and cognitive impairment after traumatic brain injury. Brain 2011, 134:449-463.
69. Knickmeyer R.C., Gouttard S., Kang C., Evans D., Wilber K., Smith J.K., Hamer R.M., Lin W., Gerig G., Gilmore J.H. A structural MRI study of human brain development from birth to 2 years. J. Neurosci. 2008, 28:12176-12182.
70. Kumar S., Yin X., Trapp B.D., Hoh J.H., Paulaitis M.E. Relating interactions between neurofilaments to the structure of axonal neurofilament distributions through polymer brush models. Biophys. J. 2002, 82:2360-2372.
71. Laplaca M.C., Prado G.R. Neuronal mechanobiology and neuronal vulnerability to traumatic loading. J. Biomech. 2010, 43:71-78.
72. Lebel C., Walker L., Leemans A., Phillips L., Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 2008, 40:1044-1055.
73. Levin H.S., Wilde E.A., Chu Z., Yallampalli R., Hanten G.R., Li X., Chia J., Vasquez C., Hunter J.V. Diffusion tensor imaging in relation to cognitive and functional outcome of traumatic brain injury in children. J. Head Trauma Rehabil. 2008, 23:197-208.
74. Liu M.C., Akle V., Zheng W., Kitlen J., O'Steen B., Larner S.F., Dave J.R., Tortella F.C., Hayes R.L., Wang K.K.W. Extensive degradation of myelin basic protein isoforms by calpain following traumatic brain injury. J. Neurochem. 2006, 98:700-712.
75. Lo C., Shifteh K., Gold T., Bello J.A., Lipton M.L. Diffusion tensor imaging abnormalities in patients with mild traumatic brain injury and neurocognitive impairment. J. Comput. Assist. Tomogr. 2009, 33:293-297.
76. Looney C.B., Smith J.K., Merck L.H., Wolfe H.M., Chescheir N.C., Hamer R.H., Gilmore J.H. Intracranial hemorrhage in asymptomatic neonates: prevalence on MR images and relationship to obstetric and neonatal risk factors. Radiology 2007, 242:535-541.
77. Lotocki G., Vaccari J.de R., Alonso O., Molano J.S., Nixon R., Deitrich W.D., Bramlett H.M. Oligodendrocyte vulnerability following traumatic brain injury in rats: Effect of moderate hypothermia. Ther. Hypotherm. Temp. Manag. 2011, 1:43-51.
78. Mahad D.J., Ziabreva I., Campbell G., Lax N., White K., Hanson P.S., Lassmann H., Turnbull D.M. Mitochondrial changes within axons in multiple sclerosis. Brain 2009, 132:1161-1174.
79. Marmarou C.R., Walker S.A., Davis C.L., Povlishock J.T. Quantitative analysis of the relationship between intra-axonal neurofilament compaction and impaired axonal transport following diffuse traumatic brain injury. J. Neurotrauma 2005, 22:1066-1080.
80. Max J.E., Lansing A.E., Koele S.L., Castillo C.S., Bokura H., Schachar R., Collings N., Williams K.E. Attention deficit hyperactivity disorder in children and adolescents following traumatic brain injury. Dev. Neuropsychol. 2004, 25:159-177.
81. Maxwell W.L., Irvine A., Graham D.I., Adams J.H., Gennarelli T.A., Tipperman R., Sturatis M. Focal axonal injury: the early axonal response to stretch. J. Neurocytol. 1991, 20:157-164.
82. Maxwell W.L., Whitfield P., Suzen B., Watt C., Graham D.I., Adams J.H., Gennarelli T.A. The cerebrovascular response to experimental lateral head acceleration. Acta Neuropathol. 1992, 84:289-296.
83. Maxwell W.L., Povlishock J.T., Graham D.I. A mechanistic analysis of non-disruptive axonal injury. A review. J. Neurotrauma 1997, 14:419-440.
84. Maxwell W.L., McCreath B.J., Graham D.I., Gennarelli T.A. Cytochemical evidence for redistribution of membrane pump calcium-ATPase and ecto-Ca-ATPase activity, and calcium influx in myelinated nerve fibres of the optic nerve after stretch injury. J. Neurocytol. 1995, 24:925-942.
85. Maxwell W.L., Domleo A., McColl G., Graham D.I. Post-acute alterations in the axonal cytoskeleton after traumatic axonal injury. J. Neurotrauma 2003, 20:151-168.
86. Maxwell W.L., MacKinnon M-A., Stewart J.E., Graham D.I. Stereology of cerebral cortex after traumatic brain injury matched to the Glasgow outcome score. Brain 2010, 133:139-160.
87. Minambres E., Ballesteros M.A., Mayorga M., Marin M.J., Munoz Figols J., Lopez-Hoyos M. Cerebral apoptosis in severe traumatic brain injury patients: an in vitro, in vivo and postmortem study. J. Neurotrauma 2008, 25:581-591.
88. Mori I., Goshima F., Mizuno T., Imai Y., Kohsaka S., Ito H., Koide K., Yoshida T., Yokochi T., Kimura Y., Nishiyama Y. Axonal injury in experimental herpes simplex encephalitis. Brain Res. 2005, 1057:186-190.
89. Muizelaar J.P., Marmarou A., Desalles A.A., et al. Cerebral blood flow and metabolism in severely head-injured children. Part 1: relationship with GCS score, outcome, ICP, and PVI. J. Neurosurg. 1989, 71:63-71.
90. Myer D.J., Gurkoff G.G., Lee S.M., Hovda D.A., Sofroniew M.V. Essential protective roles of reactive astrocytes in traumatic brain injury. Brain 2006, 129:2761-2772.
91. Namas R., Ghuma A., Hermus L., Zamora R., Okonkwo D.O., Billiar T.R., Vodovotz Y. The acute inflammatory response in trauma/hemorrhage and traumatic brain injury: Current state and emerging prospects. Libyan J. Med. 2009, 4:97-103.
92. Nimmerjahn A. Astrocytes going live: advances and challenges. J. Physiol. 2009, 587:1639-1647.
93. Parslow R.C., Morris K.P., Tasker R.C., Forsyth R.J., Hawley C.A. Epidemiology of traumatic brain injury in children receiving intensive care in the UK. Arch. Dis. Child 2005, 90:1182-1187.
94. Pettus E.H., Povlishock J.T. Characterization of a distinct set of intra-axonal ultrastructural changes associated with traumatically induced alteration in axolemmal permeability. Brain Res. 1996, 722:1-11.
95. Raja, F., Sherriff, F.E., Morris, C.S., Bridges, L.R., Esiri, M.M., 1997. Cerebral white matter damage in HIV infection demonstrated using beta-amyloid precursor protein immunoreactivity. Acta Neuropathol. (Berl) 93, 184-189.
96. Reeves T.M., Phillips L.L., Povlishock J.T. Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Exp. Neurol. 2005, 196:126-137.
97. Reiber G.D. Fatal falls in childhood. How far must children fall to sustain fatal head injury? Report of cases and review of the literature. Am. J. Forensic Med. Pathol. 1993, 14:201-207.
98. Rezaie P., Dean A. Periventricular leukomalacia: the role of inflammatory mediators and microglia pathogenesis. Neuroembryology 2002, 1:91-96.
99. Robinson, R.J., Bhuta, S. 2011. Susceptibility-weighted imaging of the brain: current utility and potential applications. J. Neuroimaging. 22, e189-e204.
100. Roessman U., Gambetti P. Pathological reaction of astrocytes in perinatal brain injury. Acta Neuropathol. 1986, 70:302-307.
101. Saatman K.E., Abai B., Grosvenor A., Vorwerk C.K., Smith D.H., Meaney D.F. Traumatic axonal injury results in biphasic calpain activation and retrograde transport impairment in mice. J. Cereb. Blood Flow Metab. 2003, 23:33-42.
102. Saatman K.E., Creed J., Raghupathi R. Calpain as a therapeutic target in traumatic brain injury. Neurotherapeutics 2010, 7:31-42.
103. Sarnat H.B., Nochlin D., Born D.E. Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in the early human fetal nervous system. Brain Dev. 1998, 20:88-94.
104. Shaw P., Kabani N.J., Lerch J.P., Eckstrand K., Lenroot R., Gogtay N., Greenstein N., Clasen L., Evans A., Rapoport J.L., Giedd J.N., Wise S.P. Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. 2008, 28:3586-3594.
105. Smith D.H., Meaney D.F. Axonal damage in traumatic brain injury. Neuroscientist 2000, 6:483-495.
106. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
107. Staal J.A., Dickson T.C., Gasperini R., Liu Y., Foa L., Vickers J.C. Initial calcium release from intracellular stores followed by calcium dysregulation is linked to secondary axotomy following transient axonal stretch injury. J. Neurochem. 2010, 112:1147-1155.
108. Staal, J.A., Vickers, J.C., 2011. Selective vulnerability of non-myelinated axons to stretch injury in an in vitro co-culture system. J. Neurotrauma, doi:10.1089/neu.2010.1658.
109. Stone J.R., Okonkwo D.O., Dialo A.O., Rubin D.G., Mutlu L.K., Povlishock J.T., Helm G.A. Impaired axonal transport and altered axolemmal permeability occur in distinct populations of damaged axons following traumatic brain injury. Exp. Neurol. 2004, 190:59-69.
110. Stys P.K. General mechanisms of axonal damage and its prevention. J. Neurolog. Sci. 2005, 233:3-13.
111. Sulaiman A., Denman N., Buchanan S., Porter N., Vesi S., Sharpe R., Graham D.I., Maxwell W.L. Stereology and ultrastructure of chronic phase axonal and cell soma pathology in stretch-injured central nerve fibers. J. Neurotrauma 2011, 28:383-400.
112. Supekar, K., Musen, M., Menon, V., 2009. Development of large-scale functional brain networks in children. PLoS Biol. 7 (7), e1000157, doi:10.1371/journal.pbio.1000157.
113. Susuki K., Rasband M. Spectrin and ankyrin-based cytoskeletons at in polarized domains in myelinated axons. Minireview. Exp. Biol. Med. 2008, 233:394-400.
114. Tamnes C.K., Østby Y., Fjell A.M., Westlye L.T., Due-Tønnessen P., Walhovd K.B. Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb. Cortex 2010, 20:534-548.
115. Tomei G., Spagnoli D., Ducati A., Landi A., Villani R., Fumagalli G., Sala C., Gennarelli T. Morphology and neurophysiology of focal axonal injury experimentally induced in the guinea pig optic nerve. Acta Neuropathol. 1990, 80:506-513.
116. Tong K.A., Ashwal S., Obenaus A., Nicherson J.P., Kido D., Haacke E.M. Susceptibility-weighted MR Imaging: a review of clinical applications in children. AJNR 2008, 29:1-9.
117. Töro{doubleacute} K., Szilvia F., György D., Pauliukevicius A., Caplinskiene M., Raudys R., Lepik D., Tuusov J., Vali M. Fatal traffic injuries among children and adolescents in three cities (capital Budapest, Vilnius, and Tallinn). J. Forensic Sci. 2011, 56:617-620.
118. Vezina Assessment of the nature and age of subdural collections in nonaccidental head injury with CT and MRI. Pediatr. Radiol. 2009, 39:586-590.
119. Venkatesan C., Chrzaszcz M.A., Choi N., Wainwright M.S. Chronic upregulation of activated microglia immunoreactive for galectin-3/Mac-2 and nerve growth factor following diffuse axonal injury. J. Neuroinflam. 2010, 7:32-42.
120. Verderio C., Matteoli M. ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFN-c. J. Immunol. 2001, 166:6383-6391.
121. von Reyn C.R., Spaethling J.M., Mesfin L.N., Ma M., Neumar R.W., Smith D.H., Siman R., Meaney D.F. Calpain mediates proteolysis of the voltage-gated sodium channel α-subunit. J. Neurosci. 2009, 29:10350-10356.
122. Voss H.U., Uluc A.M., Dyke J.P., Watts R., Kobylarz E.J., McCandliss B.D., et al. Possible axonal regrowth in late recovery from the minimally conscious state. J. Clin. Invest. 2006, 116:2005-2011.
123. Wang J., Hamm R.J., Povlishock J.T. Traumatic axonal injury in the optic nerve: evidence for axonal swelling, disconnection, dieback, and reorganization. J. Neurotrama 2011, 28:1186-1198.
124. Waxman S.G., Black J.A., Stys P.K., Ransom B.R. Ultrastructural concomitants of anoxic injury and early post-anoxic recovery in rat optic nerve. Brain Res. 1992, 574:105-119.
125. White R.E., McTigue D.M., Jakeman L.B. Regional heterogeneity in astrocyte responses following contusive spinal cord injury in mice. J. Comp. Neurol. 2010, 518:1370-1390.
126. Wilde E.A., McCauley S.R., Hunter J.V., Bigler E.D., Chu Z., Wang Z.J., et al. Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 2008, 70:948-955.
127. Williams S., Raghupathi R., Mackinnon M-A., McIntosh T.K., Saatman K.E., Graham D.I. In situ DNA fragmentation occurs in white matter up to 12 months after head injury in man. Acta Neuropathol. 2001, 102:581-590.
128. Wilson S., Raghupathi R., Saatman K.E., Mackinnon M-A., McIntosh T.K., Graham D.I. Continued in situ DNA fragmentation of microglia/macrophages in white matter weeks and months after traumatic brain injury. J. Neurotrauma 2004, 21:239-250.
129. Wolf J.A., Stys P.K., Lusardi T., Meaney D., Smith D.H. Traumatic axonal injury induces calcium influx modulated by Tetrodotoxin-sensitive sodium channels. J. Neurosci. 2001, 21:1923-1930.