Inflammation and white matter degeneration persist for years after a single traumatic brain injury

Brain

Volumn 136, Issue 1, 2013, Pages 28-42

  Johnson, Victoria E ^a   Stewart, Janice E ^b,c   Begbie, Finn D ^b   Trojanowski, John Q ^a   Smith, Douglas H ^a   Stewart, William ^b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c SOUTHERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

axonal pathology; diffuse axonal injury; inflammation; microglia; traumatic brain injury

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; CORPUS CALLOSUM; DEGENERATIVE DISEASE; FEMALE; HUMAN; HUMAN TISSUE; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; MICROGLIA; PARASAGGITAL CORTEX; PRIORITY JOURNAL; SURVIVAL TIME; TRAUMATIC BRAIN INJURY; WHITE MATTER LESION;

EID: 84873397447     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws322     Document Type: Article

References (71)

1. 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.
2. Adams JH, Graham DI, Murray LS, Scott G. Diffuse axonal injury due to nonmissile head injury in humans: an analysis of 45 cases. Ann Neurol 1982; 12: 557-63.
3. Aihara N, Hall JJ, Pitts LH, Fukuda K, Noble LJ. Altered immunoexpression of microglia and macrophages after mild head injury. J Neurotrauma 1995; 12: 53-63.
4. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol Aging 2000; 21: 383-421.
5. Brettschneider J, Libon DJ, Toledo JB, Xie SX, McCluskey L, Elman L, et al. Microglial activation and TDP-43 pathology correlate with executive dysfunction in amyotrophic lateral sclerosis. Acta Neuropathologica 2012a; 123: 395-407.
6. Brettschneider J, Toledo JB, Van Deerlin VM, Elman L, McCluskey L, Lee VM, et al. Microglial activation correlates with disease progression and upper motor neuron clinical symptoms in amyotrophic lateral sclerosis. PLoS One 2012b; 7: e39216.
7. Browne KD, Iwata A, Putt ME, Smith DH. Chronic ibuprofen administration worsens cognitive outcome following TBI in rats. Exp Neurol 2006; 201: 301-7.
8. Byrnes KR, Loane DJ, Stoica BA, Zhang J, Faden AI. Delayed mGluR5 activation limits neuroinflammation and neurodegeneration after TBI. J Neuroinflammation 2012; 9: 43.
9. Carlos TM, Clark RS, Franicola-Higgins D, Schiding JK, Kochanek PM. Expression of endothelial adhesion molecules and recruitment of neu-trophils after TBI in rats. J Leukoc Biol 1997; 61: 279-85.
10. 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 TBI. Brain Pathol 2009; 19: 214-23.
11. 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: 357-71.
12. Conde JR, Streit WJ. Microglia in the aging brain. J Neuropathol Exp Neurol 2006; 65: 199-203.
13. 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.
14. Engel S, Schluesener H, Mittelbronn M, Seid K, Adjodah D, Wehner HD, et al. Dynamics of microglial activation after human TBI are revealed by delayed expression of macrophage-related proteins MRP8 and MRP14. Acta Neuropathol 2000; 100: 313-22.
15. Fleming JC, Norenberg MD, Ramsay DA, Dekaban GA, Marcillo AE, Saenz AD, et al. The cellular inflammatory response in human spinal cords after injury. Brain 2006; 129 (Pt 12): 3249-69.
16. 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: 857-62.
17. Gale SD, Johnson SC, Bigler ED, Blatter DD. Nonspecific white matter degeneration following TBI. J Int Neuropsychol Soc 1995; 1: 17-28.
18. Geddes JF, Vowles GH, Beer TW, Ellison DW. The diagnosis of diffuse axonal injury: implications for forensic practice. Neuropathol Appl Neurobiol 1997; 23: 339-47.
19. Geddes JF, Whitwell HL, Graham DI. Traumatic axonal injury: practical issues for diagnosis in medicolegal cases. Neuropathol Appl Neurobiol 2000; 26: 105-16.
20. Gedye A, Beattie BL, Tuokko H, Horton A, Korsarek E. Severe head injury hastens age of onset of Alzheimer's disease. J Am Geriatr Soc 1989; 37: 970-3.
21. Gentleman SM, Leclercq PD, Moyes L, Graham DI, Smith C, Griffin WS, et al. Long-term intracerebral inflammatory response after TBI. Forensic Sci Int 2004; 146: 97-104.
22. 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: 139-44.
23. Graeber MB, Bise K, Mehraein P. CR3/43, a marker for activated human microglia: application to diagnostic neuropathology. Neuropathol Appl Neurobiol 1994; 20: 406-8.
24. Graham DI, Adams JH, Nicoll JA, Maxwell WL, Gennarelli TA. The nature, distribution and causes of TBI. Brain Pathol 1995a; 5: 397-406.
25. Graham DI, Gentleman SM, Lynch A, Roberts GW. Distribution of beta-amyloid protein in the brain following severe head injury. Neuropathol Appl Neurobiol 1995b; 21: 27-34.
26. Graves AB, White E, Koepsell TD, Reifler BV, van Belle G, Larson EB, et al. The association between head trauma and Alzheimer's disease. Am J Epidemiol 1990; 131: 491-501.
27. Greaves DR, Quinn CM, Seldin MF, Gordon S. Functional comparison of the murine macrosialin and human CD68 promoters in macrophage and nonmacrophage cell lines. Genomics. 1998; 54: 165-8.
28. Guo Z, Cupples LA, Kurz A, Auerbach SH, Volicer L, Chui H, et al. Head injury and the risk of AD in the MIRAGE study. Neurology 2000; 54: 1316-23.
29. Holmin S, Mathiesen T. Long-term intracerebral inflammatory response after experimental focal brain injury in rat. Neuroreport 1999; 10: 1889-91.
30. Holmin S, Mathiesen T, Shetye J, Biberfeld P. Intracerebral inflammatory response to experimental brain contusion. Acta Neurochir (Wien) 1995; 132: 110-9.
31. Holmin S, Soderlund J, Biberfeld P, Mathiesen T. Intracerebral inflammation after human brain contusion. Neurosurgery 1998; 42: 291-8; discussion 8-9.
32. 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: 1056-68.
33. Johnson VE, Stewart W, Smith DH. Traumatic brain injury and amyloid-beta pathology: a link to Alzheimer's disease? Nat Rev Neurosci 2010; 11: 361-70.
34. Johnson VE, Stewart W, Smith DH. Axonal pathology in TBI. Exp Neurol In Press.
35. Johnson VE, Stewart W, Smith DH. Widespread tau and amyloid-beta pathology many years after a single TBI in humans. Brain Pathol 2012; 22: 142-9.
36. Johnson VE, Stewart W, Trojanowski JQ, Smith DH. Acute and chronically increased immunoreactivity to phosphorylation-independent but not pathological TDP-43 after a single TBI in humans. Acta Neuropathologica 2011; 122: 715-26.
37. Leclercq PD, McKenzie JE, Graham DI, Gentleman SM. Axonal injury is accentuated in the caudal corpus callosum of head-injured patients. J Neurotrauma 2001; 18: 1-9.
38. Lenzlinger PM, Morganti-Kossmann MC, Laurer HL, McIntosh TK. The duality of the inflammatory response to TBI. Mol Neurobiol 2001; 24: 169-81.
39. Loane DJ, Byrnes KR. Role of microglia in neurotrauma. Neurotherapeutics 2010; 7: 366-77.
40. Mattiace LA, Davies P, Dickson DW. Detection of HLA-DR on microglia in the human brain is a function of both clinical and technical factors. Am J Pathol 1990; 136: 1101-14.
41. Maxwell WL, MacKinnon MA, Smith DH, McIntosh TK, Graham DI. Thalamic nuclei after human blunt head injury. J Neuropathol Exp Neurol 2006; 65: 478-88.
42. Molgaard CA, Stanford EP, Morton DJ, Ryden LA, Schubert KR, Golbeck AL. Epidemiology of head trauma and neurocognitive impairment in a multi-ethnic population. Neuroepidemiology 1990; 9: 233-42.
43. Mortimer JA, French LR, Hutton JT, Schuman LM. Head injury as a risk factor for Alzheimer's disease. Neurology 1985; 35: 264-7.
44. Mortimer JA, van Duijn CM, Chandra V, Fratiglioni L, Graves AB, Heyman A, 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): S28-35.
45. Nagamoto-Combs K, McNeal DW, Morecraft RJ, Combs CK. Prolonged microgliosis in the rhesus monkey central nervous system after TBI. J Neurotrauma 2007; 24: 1719-42.
46. Nemetz PN, Leibson C, Naessens JM, Beard M, Kokmen E, Annegers JF, et al. Traumatic brain injury and time to onset of Alzheimer's disease: a population-based study. Am J Epidemiol 1999; 149: 32-40.
47. O'Meara ES, Kukull WA, Sheppard L, Bowen JD, McCormick WC, Teri L, et al. Head injury and risk of Alzheimer's disease by apolipoprotein E genotype. Am J Epidemiol 1997; 146: 373-84.
48. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010; 6: 193-201.
49. 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: 359-69.
50. Plassman BL, Havlik RJ, Steffens DC, Helms MJ, Newman TN, Drosdick D, et al. Documented head injury in early adulthood and risk of Alzheimer's disease and other dementias. Neurology 2000; 55: 1158-66.
51. Pratico D, Trojanowski JQ. Inflammatory hypotheses: novel mechanisms of Alzheimer's neurodegeneration and new therapeutic targets? Neurobiol Aging 2000; 21: 441-5; discussion 51-3.
52. Qian L, Flood PM, Hong JS. Neuroinflammation is a key player in Parkinson's disease and a prime target for therapy. J Neural Transm 2010; 117: 971-9.
53. Ramlackhansingh AF, Brooks DJ, Greenwood RJ, Bose SK, Turkheimer FE, Kinnunen KM, et al. Inflammation after trauma: micro-glial activation and TBI. Ann Neurol 2011; 70: 374-83.
54. Ruifrok AC, Johnston DA. Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 2001; 23: 291-9.
55. Salib E, Hillier V. Head injury and the risk of Alzheimer's disease: a case control study. Int J Geriatr Psychiatry 1997; 12: 363-8.
56. Schofield PW, Tang M, Marder K, Bell K, Dooneief G, Chun M, et al. Alzheimer's disease after remote head injury: an incidence study. J Neurol Neurosurg Psychiatry 1997; 62: 119-24.
57. Sheng JG, Mrak RE, Griffin WS. Enlarged and phagocytic, but not primed, interleukin-1 alpha-immunoreactive microglia increase with age in normal human brain. Acta Neuropathol 1998; 95: 229-34.
58. Sherriff FE, Bridges LR, Sivaloganathan S. Early detection of axonal injury after human head trauma using immunocytochemistry for beta-amyloid precursor protein. Acta Neuropathol (Berl) 1994; 87: 55-62.
59. Smith DH, Chen XH, Iwata A, Graham DI. Amyloid beta accumulation in axons after TBI in humans. J Neurosurg 2003; 98: 1072-7.
60. Smith DH, Chen XH, Nonaka M, Trojanowski JQ, Lee VM, Saatman KE, 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: 982-92.
61. Soares HD, Hicks RR, Smith D, McIntosh TK. Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from TBI. J Neurosci 1995; 15: 8223-33.
62. Stahel PF, Shohami E, Younis FM, Kariya K, Otto VI, Lenzlinger PM, et al. Experimental closed head injury: analysis of neurological outcome, blood-brain barrier dysfunction, intracranial neutrophil infiltration, and neuronal cell death in mice deficient in genes for pro-inflammatory cytokines. J Cereb Blood Flow Metab 2000; 20: 369-80.
63. Stone JR, Okonkwo DO, Singleton RH, Mutlu LK, Helm GA, Povlishock JT. Caspase-3-mediated cleavage of amyloid precursor protein and formation of amyloid Beta peptide in traumatic axonal injury. J Neurotrauma 2002; 19: 601-14.
64. Sullivan P, Petitti D, Barbaccia J. Head trauma and age of onset of dementia of the Alzheimer type. JAMA 1987; 257: 2289-90.
65. Tang-Schomer MD, Johnson VE, Baas PW, Stewart W, Smith DH. Partial interruption of axonal transport due to microtubule breakage accounts for the formation of periodic varicosities after traumatic axonal injury. Exp Neurol 2012; 233: 364-72.
66. Tomaiuolo F, Bivona U, Lerch JP, Di Paola M, Carlesimo GA, Ciurli P, et al. Memory and anatomical change in severe non missile TBI: approximately 1 vs. approximately 8 years follow-up. Brain Res Bull 2012; 87: 373-82.
67. Tran HT, LaFerla FM, Holtzman DM, Brody DL. Controlled cortical impact TBI in 3xTg-AD mice causes acute intra-axonal amyloid-beta accumulation and independently accelerates the development of tau abnormalities. J Neurosci 2011a; 31: 9513-25.
68. Tran HT, Sanchez L, Esparza TJ, Brody DL. Distinct temporal and anatomical distributions of amyloid-beta and tau abnormalities following controlled cortical impact in transgenic mice. PLoS One 2011b; 6: e25475.
69. Wilson S, Raghupathi R, Saatman KE, MacKinnon MA, McIntosh TK, Graham DI. Continued in situ DNA fragmentation of microglia/macro-phages in white matter weeks and months after TBI. J Neurotrauma 2004; 21: 239-50.
70. Yoshiyama Y, Higuchi M, Zhang B, Huang SM, Iwata N, Saido TC, et al. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007; 53: 337-51.
71. Ziebell JM, Morganti-Kossmann MC. Involvement of pro-and anti-inflammatory cytokines and chemokines in the pathophysiology of TBI. Neurotherapeutics 2010; 7: 22-30.