Chronic Neurodegeneration After Traumatic Brain Injury: Alzheimer Disease, Chronic Traumatic Encephalopathy, or Persistent Neuroinflammation?

Neurotherapeutics

Volumn 12, Issue 1, 2015, Pages 143-150

  Faden, Alan I ^a   Loane, David J ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer disease; Chronic traumatic brain inflammation; Chronic traumatic encephalopathy; Concussion; Microglial activation; Neurodegeneration; Repetitive mild TBI; Traumatic brain injury

Indexed keywords

ALZHEIMER DISEASE; ANIMAL; BRAIN INJURY; BRAIN INJURY, CHRONIC; COMPLICATION; ENCEPHALITIS; HUMAN; NERVE DEGENERATION; PATHOLOGY;

ALZHEIMER DISEASE; ANIMALS; BRAIN INJURIES; BRAIN INJURY, CHRONIC; ENCEPHALITIS; HUMANS; NERVE DEGENERATION;

EID: 84928479395     PISSN: 19337213     EISSN: 18787479     Source Type: Journal    
DOI: 10.1007/s13311-014-0319-5     Document Type: Article

References (100)

1. Graves AB, White E, Koepsell TD, et al. The association between head trauma and Alzheimer's disease. Am J Epidemiol 1990;131:491-501.
2. Mortimer JA, French LR, Hutton JT, Schuman LM. Head injury as a risk factor for Alzheimer's disease. Neurology 1985;35:264-267.
3. Mortimer JA, van Duijn CM, Chandra V, et al. Head trauma as a risk factor for Alzheimer's disease: a collaborative re-analysis of case-control studies. EURODEM Risk Factors Research Group. Int J Epidemiol 1991;20(Suppl. 2):S28-S35.
4. Plassman BL, Havlik RJ, Steffens DC, et al. Documented head injury in early adulthood and risk of Alzheimer's disease and other dementias. Neurology 2000;55:1158-1166.
5. Salib E, Hillier V. Head injury and the risk of Alzheimer's disease: a case control study. Int J Geriatr Psychiatry 1997;12:363-368.
6. Wang HK, Lin SH, Sung PS, et al. Population based study on patients with traumatic brain injury suggests increased risk of dementia. J Neurol Neurosurg Psychiatry 2012;83:1080-1085.
7. Lee YK, Hou SW, Lee CC, Hsu CY, Huang YS, Su YC. Increased risk of dementia in patients with mild traumatic brain injury: a nationwide cohort study. PLoS One 2013;8:e62422.
8. Nordstrom P, Michaelsson K, Gustafson Y, Nordstrom A. Traumatic brain injury and young onset dementia: a nationwide cohort study. Ann Neurol 2014;75:374-381.
9. Omalu BI, DeKosky ST, Minster RL, Kamboh MI, Hamilton RL, Wecht CH. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery 2005;57:128-234.
10. McKee AC, Cantu RC, Nowinski CJ, et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 2009;68:709-735.
11. Omalu B, Bailes J, Hamilton RL, et al. Emerging histomorphologic phenotypes of chronic traumatic encephalopathy in American athletes. Neurosurgery 2011;69:173-183.
12. McKee AC, Stern RA, Nowinski CJ, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013;136:43-64.
13. Tate CM, Wang KK, Eonta S, et al. Serum brain biomarker level, neurocognitive performance, and self-reported symptom changes in soldiers repeatedly exposed to low-level blast: a breacher pilot study. J Neurotrauma 2013;30:1620-1630.
14. MacDonald CL, Johnson AM, Wierzechowski L, et al. Prospectively assessed clinical outcomes in concussive blast vs nonblast traumatic brain injury among evacuated US military personnel. JAMA Neurol 2014;71:994-1002.
15. MacDonald CL, Johnson AM, Nelson EC, et al. Functional status after blast-plus-impact complex concussive traumatic brain injury in evacuated United States military personnel. J Neurotrauma 2014;31:889-898.
16. Loane DJ, Faden AI. Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies. Trends Pharmacol Sci 2010;31:596-604.
17. Johnson VE, Stewart W, Smith DH. Traumatic brain injury and amyloid-beta pathology: a link to Alzheimer's disease? Nat Rev 2010;11:361-370.
18. Fratiglioni L, Ahlbom A, Viitanen M, Winblad B. Risk factors for late-onset Alzheimer's disease: a population-based, case-control study. Ann Neurol 1993;33:258-266.
19. Smith DH, Johnson VE, Stewart W. Chronic neuropathologies of single and repetitive TBI: substrates of dementia? Nat Rev Neurol 2013;9:211-221.
20. Aungst SL, Kabadi SV, Thompson SM, Stoica BA, Faden AI. Repeated mild traumatic brain injury causes chronic neuroinflammation, changes in hippocampal synaptic plasticity, and associated cognitive deficits. J Cereb Blood Flow Metab 2014;34:1223-1232.
21. Dixon CE, Kochanek PM, Yan HQ, et al. One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J Neurotrauma 1999;16:109-122.
22. Loane DJ, Kumar A, Stoica BA, Cabatbat R, Faden AI. Progressive neurodegeneration after experimental brain trauma: association with chronic microglial activation. J Neuropathol Exp Neurol 2014;73:14-29.
23. Mouzon BC, Bachmeier C, Ferro A, et al. Chronic neuropathological and neurobehavioral changes in a repetitive mild traumatic brain injury model. Ann Neurol 2014;75:241-254.
24. Pierce JE, Smith DH, Trojanowski JQ, McIntosh TK. Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 1998;87:359-369.
25. Smith DH, Chen XH, Pierce JE, et al. Progressive atrophy and neuron death for one year following brain trauma in the rat. J Neurotrauma 1997;14:715-727.
26. Bendlin BB, Ries ML, Lazar M, et al. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage 2008;42:503-514.
27. Farbota KD, Sodhi A, Bendlin BB, et al. Longitudinal volumetric changes following traumatic brain injury: a tensor-based morphometry study. J Int Neuropsychol Soc 2012;18:1006-1018.
28. Kumar R, Husain M, Gupta RK, et al. Serial changes in the white matter diffusion tensor imaging metrics in moderate traumatic brain injury and correlation with neuro-cognitive function. J Neurotrauma 2009;26:481-495.
29. Ng K, Mikulis DJ, Glazer J, et al. Magnetic resonance imaging evidence of progression of subacute brain atrophy in moderate to severe traumatic brain injury. Arch Phys Med Rehabil 2008;89(12 Suppl.):S35-S44.
30. Sidaros A, Engberg AW, Sidaros K, et al. Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: a longitudinal study. Brain 2008;131:559-572.
31. Sidaros A, Skimminge A, Liptrot MG, et al. Long-term global and regional brain volume changes following severe traumatic brain injury: a longitudinal study with clinical correlates. Neuroimage 2009;44:1-8.
32. Trivedi MA, Ward MA, Hess TM, et al. Longitudinal changes in global brain volume between 79 and 409 days after traumatic brain injury: relationship with duration of coma. J Neurotrauma 2007;24:766-771.
33. Acosta SA, Tajiri N, Shinozuka K, et al. Long-term upregulation of inflammation and suppression of cell proliferation in the brain of adult rats exposed to traumatic brain injury using the controlled cortical impact model. PLoS One 2013;8:e53376.
34. Johnson VE, Stewart JE, Begbie FD, Trojanowski JQ, Smith DH, Stewart W. Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain 2013;136:28-42.
35. Nagamoto-Combs K, McNeal DW, Morecraft RJ, Combs CK. Prolonged microgliosis in the rhesus monkey central nervous system after traumatic brain injury. J Neurotrauma 2007;24:1719-1742.
36. Nonaka M, Chen XH, Pierce JE, et al. Prolonged activation of NF-kappaB following traumatic brain injury in rats. J Neurotrauma 1999;16:1023-1034.
37. Ramlackhansingh AF, Brooks DJ, Greenwood RJ, et al. Inflammation after trauma: microglial activation and traumatic brain injury. Ann Neurol 2011;70:374-283.
38. Smith C, Gentleman SM, Leclercq PD, et al. The neuroinflammatory response in humans after traumatic brain injury. Neuropathol Appl Neurobiol 2013;39:654-666.
39. Eikelenboom P, van Exel E, Hoozemans JJ, Veerhuis R, Rozemuller AJ, van Gool WA. Neuroinflammation—an early event in both the history and pathogenesis of Alzheimer's disease. Neurodegener Dis 2010;7:38-41.
40. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010;6:193-201.
41. Saing T, Dick M, Nelson PT, Kim RC, Cribbs DH, Head E. Frontal cortex neuropathology in dementia pugilistica. J Neurotrauma 2012;29:1054-1070.
42. Byrnes KR, Loane DJ, Stoica BA, Zhang J, Faden AI. Delayed mGluR5 activation limits neuroinflammation and neurodegeneration after traumatic brain injury. J Neuroinflammation 2012;9:43.
43. Piao CS, Stoica BA, Wu J, et al. Late exercise reduces neuroinflammation and cognitive dysfunction after traumatic brain injury. Neurobiol Dis 2013;54:252-263.
44. Rodgers KM, Deming YK, Bercum FM, et al. Reversal of established traumatic brain injury-induced, anxiety-like behavior in rats after delayed, post-injury neuroimmune suppression. J Neurotrauma 2014;31:487-497.
45. Fleminger S, Oliver DL, Lovestone S, Rabe-Hesketh S, Giora A. Head injury as a risk factor for Alzheimer's disease: the evidence 10 years on; a partial replication. J Neurol Neurosurg Psychiatry 2003;74:857-862.
46. Barnes DE, Kaup A, Kirby KA, Byers AL, Diaz-Arrastia R, Yaffe K. Traumatic brain injury and risk of dementia in older veterans. Neurology 2014;83:312-319.
47. Dams-O'Connor K, Gibbons LE, Bowen JD, McCurry SM, Larson EB, Crane PK. Risk for late-life re-injury, dementia and death among individuals with traumatic brain injury: a population-based study. J Neurol Neurosurg Psychiatry 2013;84:177-182.
48. Ikonomovic MD, Uryu K, Abrahamson EE, et al. Alzheimer's pathology in human temporal cortex surgically excised after severe brain injury. Exp Neurol 2004;190:192-203.
49. Johnson VE, Stewart W, Smith DH. Widespread tau and amyloid-Beta pathology many years after a single traumatic brain injury in humans. Brain Pathol 2012;22:142-149.
50. Roberts GW, Allsop D, Bruton C. The occult aftermath of boxing. J Neurol Neurosurg Psychiatry 1990;53:373-378.
51. Roberts GW, Gentleman SM, Lynch A, Graham DI. beta A4 amyloid protein deposition in brain after head trauma. Lancet 1991;338:1422-1423.
52. Roberts GW, Gentleman SM, Lynch A, Murray L, Landon M, Graham DI. Beta amyloid protein deposition in the brain after severe head injury: implications for the pathogenesis of Alzheimer's disease. J Neurol Neurosurg Psychiatry 1994;57:419-425.
53. Hong YT, Veenith T, Dewar D, et al. Amyloid imaging with carbon 11-labeled Pittsburgh compound B for traumatic brain injury. JAMA Neurol 2014;71:23-31.
54. DeKosky ST, Abrahamson EE, Ciallella JR, et al. Association of increased cortical soluble abeta42 levels with diffuse plaques after severe brain injury in humans. Arch Neurol 2007;64:541-544.
55. Gentleman SM, Greenberg BD, Savage MJ, et al. A beta 42 is the predominant form of amyloid beta-protein in the brains of short-term survivors of head injury. Neuroreport 1997;8:1519-1522.
56. Lesne S, Koh MT, Kotilinek L, et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006;440:352-357.
57. Shankar GM, Li S, Mehta TH, et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 2008;14:837-842.
58. Walsh DM, Klyubin I, Fadeeva JV, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002;416:535-539.
59. Smith DH, Chen XH, Iwata A, Graham DI. Amyloid beta accumulation in axons after traumatic brain injury in humans. J Neurosurg 2003;98:1072-1077.
60. Sherriff FE, Bridges LR, Sivaloganathan S. Early detection of axonal injury after human head trauma using immunocytochemistry for beta-amyloid precursor protein. Acta Neuropathol 1994;87:55-62.
61. Gentleman SM, Nash MJ, Sweeting CJ, Graham DI, Roberts GW. Beta-amyloid precursor protein (beta APP) as a marker for axonal injury after head injury. Neurosci Lett 1993;160:139-144.
62. Chen XH, Johnson VE, Uryu K, Trojanowski JQ, Smith DH. A lack of amyloid beta plaques despite persistent accumulation of amyloid beta in axons of long-term survivors of traumatic brain injury. Brain Pathol 2009;19:214-223.
63. Uryu K, Chen XH, Martinez D, et al. Multiple proteins implicated in neurodegenerative diseases accumulate in axons after brain trauma in humans. Exp Neurol 2007;208:185-192.
64. Smith DH, Chen XH, 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;58:982-992.
65. Iwata A, Chen XH, McIntosh TK, Browne KD, Smith DH. Long-term accumulation of amyloid-beta in axons following brain trauma without persistent upregulation of amyloid precursor protein genes. J Neuropathol Exp Neurol 2002;61:1056-1068.
66. Chen XH, Siman R, Iwata A, Meaney DF, Trojanowski JQ, Smith DH. Long-term accumulation of amyloid-beta, beta-secretase, presenilin-1, and caspase-3 in damaged axons following brain trauma. Am J Pathol 2004;165:357-371.
67. Nath S, Agholme L, Kurudenkandy FR, Granseth B, Marcusson J, Hallbeck M. Spreading of neurodegenerative pathology via neuron-to-neuron transmission of beta-amyloid. J Neurosci 2012;32:8767-8777.
68. Horsburgh K, Cole GM, Yang F, et al. beta-amyloid (Abeta)42(43), abeta42, abeta40 and apoE immunostaining of plaques in fatal head injury. Neuropathol Appl Neurobiol 2000;26:124-132.
69. Yankner BA, Dawes LR, Fisher S, Villa-Komaroff L, Oster-Granite ML, Neve RL. Neurotoxicity of a fragment of the amyloid precursor associated with Alzheimer's disease. Science 1989;245:417-420.
70. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE. beta-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 1992;12:376-389.
71. Matsuoka Y, Picciano M, Malester B, et al. Inflammatory responses to amyloidosis in a transgenic mouse model of Alzheimer's disease. Am J Pathol 2001;158:1345-1354.
72. Loane DJ, Pocivavsek A, Moussa CE, et al. Amyloid precursor protein secretases as therapeutic targets for traumatic brain injury. Nat Med 2009;15:377-379.
73. Martland J. Punch drunk. JAMA 1928;91:1103-1107.
74. Roberts G. Brain damage in boxers: a study of the prevalence of traumatic encephalopathy amoung ex-professional boxers. Pitman, London, 1969.
75. Corsellis JA, Bruton CJ, Freeman-Browne D. The aftermath of boxing. Psychol Med 1973;3:270-303.
76. Hawkins BE, Krishnamurthy S, Castillo-Carranza DL, et al. Rapid accumulation of endogenous tau oligomers in a rat model of traumatic brain injury: possible link between traumatic brain injury and sporadic tauopathies. J Biol Chem 2013;288:17042-17050.
77. Zhou Y, Kierans A, Kenul D, et al. Mild traumatic brain injury: longitudinal regional brain volume changes. Radiology 2013;267:880-890.
78. Keightley ML, Sinopoli KJ, Davis KD, et al. Is there evidence for neurodegenerative change following traumatic brain injury in children and youth? A scoping review. Front Hum Neurosci 2014;8:139.
79. Singh R, Meier TB, Kuplicki R, et al. Relationship of collegiate football experience and concussion with hippocampal volume and cognitive outcomes. JAMA 2014;311:1883-1888.
80. Woodcock T, Morganti-Kossmann MC. The role of markers of inflammation in traumatic brain injury. Front Neurol 2013;4:18.
81. Ziebell JM, Morganti-Kossmann MC. Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 2010;7:22-30.
82. Donkin JJ, Vink R. Mechanisms of cerebral edema in traumatic brain injury: therapeutic developments. Curr Opin Neurol 2010;23:293-299.
83. Kumar A, Loane DJ. Neuroinflammation after traumatic brain injury: opportunities for therapeutic intervention. Brain Behav Immun 2012;26:1191-1201.
84. Lewis KM, Turner RJ, Vink R. Blocking neurogenic inflammation for the treatment of acute disorders of the central nervous system. Int J Inflamm 2013;2013:578480.
85. Gentleman SM, Leclercq PD, Moyes L, et al. Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci Int 2004;146:97-104.
86. Faden AI. Microglial activation and traumatic brain injury. Ann Neurol 2011;70:345-346.
87. Engel S, Schluesener H, Mittelbronn M, et al. Dynamics of microglial activation after human traumatic brain injury are revealed by delayed expression of macrophage-related proteins MRP8 and MRP14. Acta Neuropathol 2000;100:313-322.
88. Lindqvist D, Wolkowitz OM, Mellon S, et al. Proinflammatory milieu in combat-related PTSD is independent of depression and early life stress. Brain Behav Immun 2014.
89. Kumar RG, Boles JA, Wagner AK. Chronic inflammation after severe traumatic brain injury: characterization and associations with outcome at 6 and 12 months postinjury. J Head Trauma Rehabil 2014 Jun 4.
90. Juengst SB, Kumar RG, Arenth PM, Wagner AK. Exploratory associations with Tumor Necrosis Factor-alpha, disinhibition and suicidal endorsement after traumatic brain injury. Brain Behav Immun 2014;41:134-143.
91. Holmin S, Mathiesen T. Long-term intracerebral inflammatory response after experimental focal brain injury in rat. Neuroreport 1999;10:1889-1891.
92. Shitaka Y, Tran HT, Bennett RE, et al. Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity. J Neuropathol Exp Neurol 2011;70:551-567.
93. Byrnes KR, Stoica B, Loane DJ, Riccio A, Davis MI, Faden AI. Metabotropic glutamate receptor 5 activation inhibits microglial associated inflammation and neurotoxicity. Glia 2009;57:550-560.
94. Loane DJ, Stoica BA, Byrnes KR, Jeong W, Faden AI. Activation of mGluR5 and inhibition of NADPH oxidase improves functional recovery after traumatic brain injury. J Neurotrauma 2013;30:403-412.
95. Loane DJ, Stoica BA, Pajoohesh-Ganji A, Byrnes KR, Faden AI. Activation of metabotropic glutamate receptor 5 modulates microglial reactivity and neurotoxicity by inhibiting NADPH oxidase. J Biol Chem 2009;284:15629-15639.
96. Colton CA. Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 2009;4:399-418.
97. Choi SH, Aid S, Kim HW, Jackson SH, Bosetti F. Inhibition of NADPH oxidase promotes alternative and anti-inflammatory microglial activation during neuroinflammation. J Neurochem 2012;120:292-301.
98. Mannix RC, Whalen MJ. Traumatic brain injury, microglia, and beta amyloid. Int J Alzheimers Dis 2012;2012:608732.
99. Leypoldt F, Armangue T, Dalmau J. Autoimmune encephalopathies. Ann N Y Acad Sci 2014 Oct 14.
100. Leypoldt F, Wandinger KP. Paraneoplastic neurological syndromes. Clin Exp Immunol 2014;175:336-348.