The Molecular Pathophysiology of Concussive Brain Injury - an Update

Physical Medicine and Rehabilitation Clinics of North America

Volumn 27, Issue 2, 2016, Pages 373-393

  Barkhoudarian, Garni ^a   Hovda, David A ^b   Giza, Christopher C ^b  

^a JOHN WAYNE CANCER INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Concussion; Molecular mechanisms; Pathophysiology; Traumatic brain injury

Indexed keywords

GLUCOSE; GLUTAMIC ACID;

AXONAL INJURY; BRAIN BLOOD FLOW; BRAIN CONCUSSION; BRAIN METABOLISM; DIFFUSION TENSOR IMAGING; DISORDERS OF HIGHER CEREBRAL FUNCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLUCOSE METABOLISM; HUMAN; HYPOPHYSIS DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; TRAUMATIC BRAIN INJURY; ACUTE DISEASE; ANIMAL; AXON; BRAIN CIRCULATION; CHRONIC DISEASE; DIAGNOSTIC IMAGING; HYPOPHYSIS; METABOLISM; MITOCHONDRION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; RECURRENT DISEASE;

ACUTE DISEASE; ANIMALS; AXONS; BRAIN CONCUSSION; CEREBROVASCULAR CIRCULATION; CHRONIC DISEASE; DIFFUSION TENSOR IMAGING; GLUCOSE; GLUTAMIC ACID; HUMANS; MAGNETIC RESONANCE IMAGING; MITOCHONDRIA; PITUITARY GLAND; RECURRENCE;

EID: 84964645617     PISSN: 10479651     EISSN: 15581381     Source Type: Journal    
DOI: 10.1016/j.pmr.2016.01.003     Document Type: Review

References (156)

1. Kelly J.P., Nichols J.S., Filley C.M., et al. Concussion in sports. Guidelines for the prevention of catastrophic outcome. JAMA 1991, 266(20):2867-2869.
2. Guskiewicz K.M., McCrea M., Marshall S.W., et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA concussion study. JAMA 2003, 290(19):2549-2555.
3. Langlois J.A., Rutland-Brown W., Wald M.M. The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil 2006, 21(5):375-378.
4. Practice parameter: the management of concussion in sports (summary statement). Report of the Quality Standards Subcommittee. Neurology 1997, 48(3):581-585.
5. Giza C.C., Kutcher J.S., Ashwal S., et al. Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the guideline development subcommittee of the American Academy of Neurology. Neurology 2013, 80(24):2250-2257.
6. Barr W., McCrea M. Sensitivity and specificity of standardized neurocognitive testing immediately following sports concussion. J Int Neuropsychol Soc 2001, 7(6):693.
7. McCrory P., Meeuwisse W., Johnston K., et al. Consensus statement on concussion in sport: the 3rd international conference on concussion in sport held in Zurich, November 2008. Br J Sports Med 2009, 43(Suppl 1):i76-i90.
8. Vagnozzi R., Signoretti S., Tavazzi B., et al. Hypothesis of the postconcussive vulnerable brain: experimental evidence of its metabolic occurrence. Neurosurgery 2005, 57(1):164-171. [discussion: 164-71].
9. Vagnozzi R., Tavazzi B., Signoretti S., et al. Temporal window of metabolic brain vulnerability to concussions: mitochondrial-related impairment-part I. Neurosurgery 2007, 61(2):379-388. [discussion: 388-9].
10. Longhi L., Saatman K.E., Fujimoto S., et al. Temporal window of vulnerability to repetitive experimental concussive brain injury. Neurosurgery 2005, 56(2):364-374. [discussion: 364-74].
11. Prins M.L., Hales A., Reger M.L., et al. Repeat traumatic brain injury in the juvenile rat is associated with increased axonal injury and cognitive impairments. Dev Neurosci 2010, 32(4):510-518.
12. Giza C.C., Maria N.S., Hovda D.A. N-methyl-D-aspartate receptor subunit changes after traumatic injury to the developing brain. J Neurotrauma 2006, 23(6):950-961.
13. Gurkoff G.G., Giza C.C., Shin D., et al. Acute neuroprotection to pilocarpine-induced seizures is not sustained after traumatic brain injury in the developing rat. Neuroscience 2009, 164(2):862-876.
14. DeFord S.M., Wilson M.S., Rice A.C., et al. Repeated mild brain injuries result in cognitive impairment in B6C3F1 mice. J Neurotrauma 2002, 19(4):427-438.
15. Henninger N., Sicard K.M., Li Z., 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 2007, 35(11):2607-2614.
16. Prins M.L., Hovda D.A. The effects of age and ketogenic diet on local cerebral metabolic rates of glucose after controlled cortical impact injury in rats. J Neurotrauma 2009, 26(7):1083-1093.
17. Difiori J.P., Giza C.C. New techniques in concussion imaging. Curr Sports Med Rep 2010, 9(1):35-39.
18. Hillered L., Vespa P.M., Hovda D.A. Translational neurochemical research in acute human brain injury: the current status and potential future for cerebral microdialysis. J Neurotrauma 2005, 22(1):3-41.
19. Vespa P., Bergsneider M., Hattori N., et al. Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J Cereb Blood Flow Metab 2005, 25(6):763-774.
20. Barkhoudarian G., Hovda D., Giza C. The molecular pathophysiology of concussive brain injury. Clin Sports Med 2011, 30(1):33.
21. Farkas O., Lifshitz J., Povlishock J.T. Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury?. J Neurosci 2006, 26(12):3130-3140.
22. Faden A.I., Demediuk P., Panter S.S., et al. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 1989, 244(4906):798-800.
23. Kawamata T., Katayama Y., Hovda D.A., et al. Administration of excitatory amino acid antagonists via microdialysis attenuates the increase in glucose utilization seen following concussive brain injury. J Cereb Blood Flow Metab 1992, 12(1):12-24.
24. Yoshino A., Hovda D.A., Kawamata T., et al. Dynamic changes in local cerebral glucose utilization following cerebral conclusion in rats: evidence of a hyper- and subsequent hypometabolic state. Brain Res 1991, 561(1):106-119.
25. Giza C.C., Hovda D.A. The neurometabolic cascade of concussion. J Athl Train 2001, 36(3):228-235.
26. Kubota M., Nakamura T., Sunami K., et al. Changes of local cerebral glucose utilization, DC potential and extracellular potassium concentration in experimental head injury of varying severity. Neurosurg Rev 1989, 12(Suppl 1):393-399.
27. Somjen G.G., Giacchino J.L. Potassium and calcium concentrations in interstitial fluid of hippocampal formation during paroxysmal responses. J Neurophysiol 1985, 53(4):1098-1108.
28. Fabricius M., Fuhr S., Willumsen L., et al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol 2008, 119(9):1973-1984.
29. Hartings J.A., Strong A.J., Fabricius M., et al. Spreading depolarizations and late secondary insults after traumatic brain injury. J Neurotrauma 2009, 26(11):1857-1866.
30. Strong A.J., Fabricius M., Boutelle M.G., et al. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 2002, 33(12):2738-2743.
31. Leao A.A. Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol 1947, 10(6):409-414.
32. Verweij B.H., Muizelaar J.P., Vinas F.C., et al. Mitochondrial dysfunction after experimental and human brain injury and its possible reversal with a selective N-type calcium channel antagonist (SNX-111). Neurol Res 1997, 19(3):334-339.
33. Xiong Y., Gu Q., Peterson P.L., et al. Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J Neurotrauma 1997, 14(1):23-34.
34. Kawamata T., Katayama Y., Hovda D.A., et al. Lactate accumulation following concussive brain injury: the role of ionic fluxes induced by excitatory amino acids. Brain Res 1995, 674(2):196-204.
35. Kalimo H., Rehncrona S., Soderfeldt B. The role of lactic acidosis in the ischemic nerve cell injury. Acta Neuropathol 1981, 7:20-22.
36. Magistretti P.J., Pellerin L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc Lond 1999, 354(1387):1155-1163.
37. Schurr A., Payne R.S. Lactate, not pyruvate, is neuronal aerobic glycolysis end product: an in vitro electrophysiological study. Neuroscience 2007, 147(3):613-619.
38. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J Neurosci 1996, 16(3):877-885.
39. Bouzat P., Sala N., Suys T., et al. Cerebral metabolic effects of exogenous lactate supplementation on the injured human brain. Intensive Care Med 2014, 40(3):412.
40. Schurr A., Gozal E. Aerobic production and utilization of lactate satisfy increased energy demands upon neuronal activation in hippocampal slices and provide neuroprotection against oxidative stress. Front Pharmacol 2011, 2:96.
41. Andersen B.J., Marmarou A. Post-traumatic selective stimulation of glycolysis. Brain Res 1992, 585(1-2):184-189.
42. Sunami K., Nakamura T., Ozawa Y., et al. Hypermetabolic state following experimental head injury. Neurosurg Rev 1989, 12(Suppl 1):400-411.
43. Yoshino A., Hovda D.A., Katayama Y., et al. Hippocampal CA3 lesion prevents postconcussive metabolic dysfunction in CA1. J Cereb Blood Flow Metab 1992, 12(6):996-1006.
44. Bergsneider M., Hovda D.A., Shalmon E., et al. Cerebral hyperglycolysis following severe traumatic brain injury in humans: a positron emission tomography study. J Neurosurg 1997, 86(2):241-251.
45. Peskind E.R., Petrie E.C., Cross D.J., et al. Cerebrocerebellar hypometabolism associated with repetitive blast exposure mild traumatic brain injury in 12 Iraq war veterans with persistent post-concussive symptoms. Neuroimage 2011, 54(Suppl 1):S76.
46. Provenzano F., Jordan B., Tikofsky R., et al. F-18 FDG PET imaging of chronic traumatic brain injury in boxers: a statistical parametric analysis. Nucl Med Commun 2010, 31(11):952.
47. Byrnes K.R., Wilson C.M., Brabazon F., et al. FDG-PET imaging in mild traumatic brain injury: a critical review. Front Neuroenergetics 2013, 5:13.
48. Lifshitz J., Sullivan P.G., Hovda D.A., et al. Mitochondrial damage and dysfunction in traumatic brain injury. Mitochondrion 2004, 4(5-6):705-713.
49. Robertson C.L., Saraswati M., Fiskum G. Mitochondrial dysfunction early after traumatic brain injury in immature rats. J Neurochem 2007, 101(5):1248-1257.
50. Hovda D.A., Yoshino A., Kawamata T., et al. Diffuse prolonged depression of cerebral oxidative metabolism following concussive brain injury in the rat: a cytochrome oxidase histochemistry study. Brain Res 1991, 567(1):1-10.
51. Signoretti S., Di Pietro V., Vagnozzi R., et al. Transient alterations of creatine, creatine phosphate, N-acetylaspartate and high-energy phosphates after mild traumatic brain injury in the rat. Mol Cell Biochem 2010, 333(1-2):269-277.
52. Vagnozzi R., Signoretti S., Tavazzi B., et al. Temporal window of metabolic brain vulnerability to concussion: a pilot 1H-magnetic resonance spectroscopic study in concussed athletes-part III. Neurosurgery 2008, 62(6):1286-1295. [discussion: 1295-6].
53. Appelberg K.S., Hovda D.A., Prins M.L. The effects of a ketogenic diet on behavioral outcome after controlled cortical impact injury in the juvenile and adult rat. J Neurotrauma 2009, 26(4):497-506.
54. Arun P., Ariyannur P.S., Moffett J.R., et al. Metabolic acetate therapy for the treatment of traumatic brain injury. J Neurotrauma 2010, 27(1):293-298.
55. Prins M.L., Fujima L.S., Hovda D.A. Age-dependent reduction of cortical contusion volume by ketones after traumatic brain injury. J Neurosci Res 2005, 82(3):413-420.
56. Davis L.M., Pauly J.R., Readnower R.D., et al. Fasting is neuroprotective following traumatic brain injury. J Neurosci Res 2008, 86(8):1812-1822.
57. Cantu R.C. Second-impact syndrome. Clin Sports Med 1998, 17(1):37-44.
58. McCrory P.R., Berkovic S.F. Second impact syndrome. Neurology 1998, 50(3):677-683.
59. Martin N.A., Patwardhan R.V., Alexander M.J., et al. Characterization of cerebral hemodynamic phases following severe head trauma: hypoperfusion, hyperemia, and vasospasm. J Neurosurg 1997, 87(1):9-19.
60. Coles J.P., Fryer T.D., Smielewski P., et al. Incidence and mechanisms of cerebral ischemia in early clinical head injury. J Cereb Blood Flow Metab 2004, 24(2):202-211.
61. Maugans T.A., Farley C., Altaye M., et al. Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics 2012, 129(1):28.
62. Meier T., Bellgowan P., Singh R., et al. Recovery of cerebral blood flow following sports-related concussion. JAMA Neurol 2015, 72(5):530-538.
63. Bartnik-Olson B., Holshouser B., Wang H., et al. Impaired neurovascular unit function contributes to persistent symptoms after concussion: a pilot study. J Neurotrauma 2014, 31(17):1497.
64. Immonen R., Heikkinen T., Tahtivaara L., et al. Cerebral blood volume alterations in the perilesional areas in the rat brain after traumatic brain injury-comparison with behavioral outcome. J Cereb Blood Flow Metab 2010, 30(7):1318-1328.
65. Pasco A., Lemaire L., Franconi F., et al. Perfusional deficit and the dynamics of cerebral edemas in experimental traumatic brain injury using perfusion and diffusion-weighted magnetic resonance imaging. J Neurotrauma 2007, 24(8):1321-1330.
66. Mata M., Staple J., Fink D.J. Changes in intra-axonal calcium distribution following nerve crush. J Neurobiol 1986, 17(5):449-467.
67. Maxwell W.L., McCreath B.J., Graham D.I., et al. 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(12):925-942.
68. Johnson G.V., Greenwood J.A., Costello A.C., et al. The regulatory role of calmodulin in the proteolysis of individual neurofilament proteins by calpain. Neurochem Res 1991, 16(8):869-873.
69. Nakamura Y., Takeda M., Angelides K.J., et al. Effect of phosphorylation on 68 KDa neurofilament subunit protein assembly by the cyclic AMP dependent protein kinase in vitro. Biochem Biophys Res Commun 1990, 169(2):744-750.
70. Nixon R.A. The regulation of neurofilament protein dynamics by phosphorylation: clues to neurofibrillary pathobiology. Brain Pathol 1993, 3(1):29-38.
71. Sternberger N.H., Sternberger L.A. Neurotypy: the heterogeneity of brain proteins. Ann N Y Acad Sci 1983, 420:90-99.
72. Maxwell W.L., Povlishock J.T., Graham D.L. A mechanistic analysis of nondisruptive axonal injury: a review. J Neurotrauma 1997, 14(7):419-440.
73. 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(1-2):1-11.
74. Povlishock J.T., Pettus E.H. Traumatically induced axonal damage: evidence for enduring changes in axolemmal permeability with associated cytoskeletal change. Acta Neurochir Suppl 1996, 66:81-86.
75. Saatman K.E., Abai B., Grosvenor A., et al. Traumatic axonal injury results in biphasic calpain activation and retrograde transport impairment in mice. J Cereb Blood Flow Metab 2003, 23(1):34-42.
76. Spain A., Daumas S., Lifshitz J., et al. Mild fluid percussion injury in mice produces evolving selective axonal pathology and cognitive deficits relevant to human brain injury. J Neurotrauma 2010, 27(8):1429.
77. Smith D.H., Johnson V.E., Stewart W. Chronic neuropathologies of single and repetitive TBI: substrates of dementia?. Nat Rev Neurol 2013, 9(4):211-221.
78. Mac Donald C.L., Dikranian K., Bayly P., et al. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J Neurosci 2007, 27(44):11869-11876.
79. Benson R.R., Meda S.A., Vasudevan S., et al. Global white matter analysis of diffusion tensor images is predictive of injury severity in traumatic brain injury. J Neurotrauma 2007, 24(3):446-459.
80. Wilde E.A., McCauley S.R., Hunter J.V., et al. Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 2008, 70(12):948-955.
81. Miles L., Grossman R., Johnson G., et al. Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj 2008, 22(2):115.
82. Niogi S.N., Mukherjee P., Ghajar J., 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. AJNR Am J Neuroradiol 2008, 29(5):967-973.
83. Lipton M.L., Gellella E., Lo C., et al. Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. J Neurotrauma 2008, 25(11):1335-1342.
84. Wozniak J.R., Krach L., Ward E., et al. Neurocognitive and neuroimaging correlates of pediatric traumatic brain injury: a diffusion tensor imaging (DTI) study. Arch Clin Neuropsychol 2007, 22(5):555-568.
85. Mayer A., Ling J., Yang Z., et al. Diffusion abnormalities in pediatric mild traumatic brain injury. J Neurosci 2012, 32(50):17961.
86. Dennis E.L., Ellis M.U., Marion S.D., et al. Callosal function in pediatric traumatic brain injury linked to disrupted white matter integrity. J Neurosci 2015, 35(28):10202-10211.
87. Ellis M.U., Marion S.D., McArthur D.L., et al. The UCLA study of children with moderate-to-severe traumatic brain injury: event-related potential measure of interhemispheric transfer time. J Neurotrauma 2015, [Epub ahead of print].
88. Niogi S.N., Mukherjee P., Ghajar J., et al. Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain 2008, 131(Pt 12):3209-3221.
89. Cull-Candy S., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 2001, 11(3):327-335.
90. Liu L., Wong T.P., Pozza M.F., et al. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 2004, 304(5673):1021-1024.
91. Tang Y.P., Wang H., Feng R., et al. Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology 2001, 41(6):779-790.
92. Reeves T.M., Lyeth B.G., Povlishock J.T. Long-term potentiation deficits and excitability changes following traumatic brain injury. Exp Brain Res 1995, 106(2):248-256.
93. Sick T.J., Perez-Pinzon M.A., Feng Z.Z. Impaired expression of long-term potentiation in hippocampal slices 4 and 48 h following mild fluid-percussion brain injury in vivo. Brain Res 1998, 785(2):287-292.
94. Sanders M.J., Sick T.J., Perez-Pinzon M.A., et al. Chronic failure in the maintenance of long-term potentiation following fluid percussion injury in the rat. Brain Res 2000, 861(1):69-76.
95. Jantzen K.J., Anderson B., Steinberg F.L., et al. A prospective functional MR imaging study of mild traumatic brain injury in college football players. AJNR Am J Neuroradiol 2004, 25(5):738-745.
96. Pardini J., Pardini D., Becker J., et al. Postconcussive symptoms are associated with compensatory cortical recruitment during a working memory task. Neurosurgery 2010, 67(4):1020.
97. Lovell M.R., Pardini J.E., Welling J., et al. Functional brain abnormalities are related to clinical recovery and time to return-to-play in athletes. Neurosurgery 2007, 61(2):352-359. [discussion: 359-60].
98. McAllister T.W., Sparling M.B., Flashman L.A., et al. Neuroimaging findings in mild traumatic brain injury. J Clin Exp Neuropsychol 2001, 23(6):775-791.
99. Kissick J., Johnston K.M. Return to play after concussion: principles and practice. Clin J Sport Med 2005, 15(6):426-431.
100. Putukian M. Repeat mild traumatic brain injury: how to adjust return to play guidelines. Curr Sports Med Rep 2006, 5(1):15-22.
101. Cantu R.C., Gean A.D. Second-impact syndrome and a small subdural hematoma: an uncommon catastrophic result of repetitive head injury with a characteristic imaging appearance. J Neurotrauma 2010, 27(9):1557.
102. Mori T., Katayama Y., Kawamata T. Acute hemispheric swelling associated with thin subdural hematomas: pathophysiology of repetitive head injury in sports. Acta Neurochir Suppl 2006, 96:40.
103. McCrory P., Davis G., Makdissi M. Second impact syndrome or cerebral swelling after sporting head injury. Curr Sports Med Rep 2012, 11(1):21.
104. Tavazzi B., Vagnozzi R., Signoretti S., et al. Temporal window of metabolic brain vulnerability to concussions: oxidative and nitrosative stresses-part II. Neurosurgery 2007, 61(2):390-395. [discussion: 395-6].
105. Meehan W., Zhang J., Mannix R., et al. Increasing recovery time between injuries improves cognitive outcome after repetitive mild concussive brain injuries in mice. Neurosurgery 2012, 71(4):885.
106. Mannix R., Meehan W., Mandeville J., et al. Clinical correlates in an experimental model of repetitive mild brain injury. Ann Neurol 2013, 74(1):65.
107. Prins M.L., Alexander D., Giza C.C., et al. Repeated mild traumatic brain injury: mechanisms of cerebral vulnerability. J Neurotrauma 2013, 30(1):30.
108. Vagnozzi R., Signoretti S., Cristofori L., et al. Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multicentre, proton magnetic resonance spectroscopic study in concussed patients. Brain 2010, 133(11):3232.
109. Vespa P., Boonyaputthikul R., McArthur D.L., et al. Intensive insulin therapy reduces microdialysis glucose values without altering glucose utilization or improving the lactate/pyruvate ratio after traumatic brain injury. Crit Care Med 2006, 34(3):850-856.
110. Tremblay S., Beaulé V., Proulx S., et al. Multimodal assessment of primary motor cortex integrity following sport concussion in asymptomatic athletes. Clin Neurophysiol 2014, 125(7):1371.
111. Gardner A., Iverson G., Stanwell P. A systematic review of proton magnetic resonance spectroscopy findings in sport-related concussion. J Neurotrauma 2014, 31(1):1.
112. Huang M.X., Theilmann R.J., Robb A., et al. Integrated imaging approach with MEG and DTI to detect mild traumatic brain injury in military and civilian patients. J Neurotrauma 2009, 26(8):1213-1226.
113. Levin H.S., Wilde E., Troyanskaya M., et al. Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. J neurotrauma 2010, 27(4):683-694.
114. Schrader H., Mickeviciene D., Gleizniene R., et al. Magnetic resonance imaging after most common form of concussion. BMC Med Imaging 2009, 9:11.
115. Laurer H.L., Bareyre F.M., Lee V.M., et al. Mild head injury increasing the brain's vulnerability to a second concussive impact. J Neurosurg 2001, 95(5):859-870.
116. Mouzon B., Chaytow H., Crynen G., et al. Repetitive mild traumatic brain injury in a mouse model produces learning and memory deficits accompanied by histological changes. J Neurotrauma 2012, 29(18):2761.
117. DeRoss A.L., Adams J.E., Vane D.W., et al. Multiple head injuries in rats: effects on behavior. J Trauma 2002, 52(4):708-714.
118. Uryu K., Laurer H., McIntosh T., et al. Repetitive mild brain trauma accelerates Aβ deposition, lipid peroxidation, and cognitive impairment in a transgenic mouse model of Alzheimer amyloidosis. J Neurosci 2002, 22(2):446-454.
119. Rabadi M.H., Jordan B.D. The cumulative effect of repetitive concussion in sports. Clin J Sport Med 2001, 11(3):194-198.
120. Smith D.H., Nakamura M., McIntosh T.K., et al. Brain trauma induces massive hippocampal neuron death linked to a surge in beta-amyloid levels in mice overexpressing mutant amyloid precursor protein. Am J Pathol 1998, 153(3):1005-1010.
121. Critchley M. Medical aspects of boxing, particularly from a neurological standpoint. Br Med J 1957, 1(5015):357.
122. Martland, Harrison S. Punch drunk. JAMA 1928, 91:1103-1107.
123. McKee A.C., Cantu R.C., Nowinski C.J., et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 2009, 68(7):709-735.
124. Omalu B.I., Hamilton R.L., Kamboh M.I., et al. Chronic traumatic encephalopathy (CTE) in a National Football League player: case report and emerging medicolegal practice questions. J Forensic Nurs 2010, 6(1):40-46.
125. Smith C., Graham D.I., Murray L.S., et al. Tau immunohistochemistry in acute brain injury. Neuropathol Appl Neurobiol 2003, 29(5):496-502.
126. McKee A.C., Cairns N.J., Dickson D.W., et al. The first NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. Acta Neuropathol 2016, 131(1):75-86.
127. Genis L., Chen Y., Shohami E., et al. Tau hyperphosphorylation in apolipoprotein E-deficient and control mice after closed head injury. J Neurosci Res 2000, 60(4):559-564.
128. Hoshino S., Tamaoka A., Takahashi M., et al. Emergence of immunoreactivities for phosphorylated tau and amyloid-beta protein in chronic stage of fluid percussion injury in rat brain. Neuroreport 1998, 9(8):1879-1883.
129. Kanayama G., Takeda M., Niigawa H., et al. The effects of repetitive mild brain injury on cytoskeletal protein and behavior. Methods Find Exp Clin Pharmacol 1996, 18(2):105-115.
130. Smith D.H., Chen X.H., Nonaka M., et al. Accumulation of amyloid beta and tau and the formation of neurofilament inclusions following diffuse brain injury in the pig. J Neuropathol Exp Neurol 1999, 58(9):982-992.
131. McKee A.C., Stein T.D., Nowinski C.J., et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013, 136(1):43.
132. Omalu B., Bailes J., Hamilton R., et al. Emerging histomorphologic phenotypes of chronic traumatic encephalopathy in American athletes. Neurosurgery 2011, 69(1):173.
133. Hazrati L.-N., Tartaglia M.C., Diamandis P., et al. Absence of chronic traumatic encephalopathy in retired football players with multiple concussions and neurological symptomatology. Front Hum Neurosci 2013, 7:222.
134. Bieniek K.F., Ross O.A., Cormier K.A., et al. Chronic traumatic encephalopathy pathology in a neurodegenerative disorders brain bank. Acta Neuropathol 2015, 130(6):877-889.
135. Jordan B.D. Chronic traumatic brain injury associated with boxing. Semin Neurol 2000, 20(2):179-185.
136. Jordan B.D., Relkin N.R., Ravdin L.D., et al. Apolipoprotein E epsilon4 associated with chronic traumatic brain injury in boxing. JAMA 1997, 278(2):136-140.
137. Hartman R.E., Laurer H., Longhi L., et al. Apolipoprotein E4 influences amyloid deposition but not cell loss after traumatic brain injury in a mouse model of Alzheimer's disease. J Neurosci 2002, 22(23):10083-10087.
138. Zhang L., Heier L.A., Zimmerman R.D., et al. Diffusion anisotropy changes in the brains of professional boxers. AJNR Am J Neuroradiol 2006, 27(9):2000-2004.
139. Guskiewicz K.M., Marshall S.W., Bailes J., et al. Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery 2005, 57(4):719-726. [discussion: 719-26].
140. Guskiewicz K.M., Marshall S.W., Bailes J., et al. Recurrent concussion and risk of depression in retired professional football players. Med Sci Sports Exerc 2007, 39(6):903-909.
141. Agha A., Rogers B., Sherlock M., et al. Anterior pituitary dysfunction in survivors of traumatic brain injury. J Clin Endocrinol Metab 2004, 89(10):4929-4936.
142. Aimaretti G., Ambrosio M.R., Di Somma C., et al. Traumatic brain injury and subarachnoid haemorrhage are conditions at high risk for hypopituitarism: screening study at 3 months after the brain injury. Clin Endocrinol 2004, 61(3):320-326.
143. Aimaretti G., Ambrosio M.R., Di Somma C., et al. Residual pituitary function after brain injury-induced hypopituitarism: a prospective 12-month study. J Clin Endocrinol Metab 2005, 90(11):6085-6092.
144. Bondanelli M., De Marinis L., Ambrosio M.R., et al. Occurrence of pituitary dysfunction following traumatic brain injury. J Neurotrauma 2004, 21(6):685-696.
145. Herrmann B.L., Rehder J., Kahlke S., et al. Hypopituitarism following severe traumatic brain injury. Exp Clin Endocrinol Diabetes 2006, 114(6):316-321.
146. Kelly D.F., Gonzalo I.T., Cohan P., et al. Hypopituitarism following traumatic brain injury and aneurysmal subarachnoid hemorrhage: a preliminary report. J Neurosurg 2000, 93(5):743-752.
147. Leal-Cerro A., Flores J.M., Rincon M., et al. Prevalence of hypopituitarism and growth hormone deficiency in adults long-term after severe traumatic brain injury. Clin Endocrinol 2005, 62(5):525-532.
148. Lieberman S.A., Oberoi A.L., Gilkison C.R., et al. Prevalence of neuroendocrine dysfunction in patients recovering from traumatic brain injury. J Clin Endocrinol Metab 2001, 86(6):2752-2756.
149. Tanriverdi F., Senyurek H., Unluhizarci K., et al. High risk of hypopituitarism after traumatic brain injury: a prospective investigation of anterior pituitary function in the acute phase and 12 months after trauma. J Clin Endocrinol Metab 2006, 91(6):2105-2111.
150. Ware J., Sherbourne C., The M.O.S. 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Med Care 1992, 30(6):473.
151. Ware J.E., Kosinski M. SF-36 physical & mental health summary scales: a manual for users of version 1 2001, Quality Metric, Lincoln (RI).
152. Bavisetty S., McArthur D., Dusick J., et al. Chronic hypopituitarism after traumatic brain injury: risk assessment and relationship to outcome. Neurosurgery 2008, 62(5):1080.
153. Kelly D., Chaloner C., Evans D., et al. Prevalence of pituitary hormone dysfunction, metabolic syndrome, and impaired quality of life in retired professional football players: a prospective study. J Neurotrauma 2014, 31(13):1161.
154. Greco T., Hovda D., Prins M. The effects of repeat traumatic brain injury on the pituitary in adolescent rats. J Neurotrauma 2013, 30(23):1983.
155. Kornblum R., Fisher R. Pituitary lesions in craniocerebral injuries. Arch Pathol 1969, 88(3):242.
156. Ceballos R. Pituitary changes in head trauma (analysis of 102 consecutive cases of head injury). Ala J Med Sci 1966, 3(2):185.