Neurodegeneration and sport

Neurosurgery

Volumn 76, Issue 6, 2015, Pages 643-655

  Davis, Gavin A ^a,b   Castellani, Rudolph J ^c   McCrory, Paul ^b  

^a CABRINI INSTITUTE   (Australia)

^b FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

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

Author keywords

Chronic traumatic encephalopathy; Concussion; Sport; Tauopathy; Traumatic brain injury

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; OPIATE; TAR DNA BINDING PROTEIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; ATHLETE; CHRONIC DISEASE; CLINICAL FEATURE; CONCUSSION; CONTACT SPORT; DEGENERATIVE DISEASE; DISEASE CLASSIFICATION; FRONTOTEMPORAL DEMENTIA; HUMAN; NEUROPATHOLOGY; OPIATE ADDICTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; RISK; SPORT INJURY; SYSTEMATIC REVIEW (TOPIC); TAUOPATHY; TRAUMATIC BRAIN INJURY; ATHLETIC INJURIES; BRAIN; BRAIN CONCUSSION; BRAIN INJURY, CHRONIC; COMPLICATION; NEURODEGENERATIVE DISEASES; PATHOLOGY; SPORT;

AGING; ATHLETES; ATHLETIC INJURIES; BRAIN; BRAIN CONCUSSION; BRAIN INJURY, CHRONIC; HUMANS; NEURODEGENERATIVE DISEASES; SPORTS;

EID: 84929687707     PISSN: 0148396X     EISSN: 15244040     Source Type: Journal    
DOI: 10.1227/NEU.0000000000000722     Document Type: Review

References (101)

1. 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(7):709-735.
2. McKee AC, Gavett BE, Stern RA, et al. TDP-43 proteinopathy and motor neuron disease in chronic traumatic encephalopathy. J Neuropathol Exp Neurol. 2010;69(9):918-929.
3. McKee AC, Stern RA, Nowinski CJ, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain. 2013;136(pt 1):43-64.
4. Omalu BI, Bailes J, Hammers JL, Fitzsimmons RP. Chronic traumatic encephalopathy, suicides and parasuicides in professional American athletes: the role of the forensic pathologist. Am J Forensic Med Pathol. 2010;31(2): 130-132.
5. Omalu BI, DeKosky ST, Minster RL, Kamboh MI, Hamilton RL, Wecht CH. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery. 2005;57(1):128-134; discussion 128-134.
6. NFL retired players Mediation Agreement. Available at: http://static.nfl.com/static/content/public/photo/2013/08/29/0ap2000000235504.pdf. Accessed August 16, 2014.
7. Barr WB. An evidence based approach to sports concussion: confronting the availability cascade. Neuropsychol Rev. 2013;23(4):271-272.
8. Solomon GS, Sills A. Chronic traumatic encephalopathy and the availability cascade. Phys Sportsmed. 2014;42(3):26-31.
9. Randolph C. Is chronic traumatic encephalopathy a real disease? Curr Sports Med Rep. 2014;13(1):33-37.
10. Martland HS. Punch drunk. JAMA. 1928;91(15):1103-1107.
11. Gardner A, Iverson GL, McCrory P. Chronic traumatic encephalopathy in sport: a systematic review. Br J Sports Med. 2014;48(2):84-90.
12. McCrory P, Zazryn T, Cameron P. The evidence for chronic traumatic encephalopathy in boxing. Sports Med. 2007;37(6):467-476.
13. McCrory P. Boxing and the risk of chronic brain injury. BMJ. 2007;335(7624): 781-782.
14. Braak H, Thal DR, Ghebremedhin E, Del Tredici K. Stages of the pathologic process in Alzheimer disease: age categories from 1 to 100 years. J Neuropathol Exp Neurol. 2011;70(11):960-969.
15. Iverson GL. Chronic traumatic encephalopathy and risk of suicide in former athletes. Br J Sports Med. 2014;48(2):162-165.
16. Hazrati LN, Tartaglia MC, 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.
17. Omalu B, Bailes J, Hamilton RL, et al. Emerging histomorphologic phenotypes of chronic traumatic encephalopathy in American athletes. Neurosurgery. 2011;69 (1):173-183; discussion 183.
18. Montenigro PH, Baugh CM, Daneshvar DH, et al. Clinical subtypes of chronic traumatic encephalopathy: literature review and proposed research diagnostic criteria for traumatic encephalopathy syndrome. Alzheimers Res Ther. 2014;6(5):68.
19. Stern RA, Daneshvar DH, Baugh CM, et al. Clinical presentation of chronic traumatic encephalopathy. Neurology. 2013;81(13):1122-1129.
20. Jordan BD. The clinical spectrum of sport-related traumatic brain injury. Nat Rev Neurol. 2013;9(4):222-230.
21. Baron SL, Hein MJ, Lehman E, Gersic CM. Body mass index, playing position, race, and the cardiovascular mortality of retired professional football players. Am J Cardiol. 2012;109(6):889-896.
22. Anthony IC, Norrby KE, Dingwall T, et al. Predisposition to accelerated Alzheimer-related changes in the brains of human immunodeficiency virus negative opiate abusers. Brain. 2010;133(pt 12):3685-3698.
23. Oyanagi K, Makifuchi T, Ohtoh T, et al. Amyotrophic lateral sclerosis of Guam: the nature of the neuropathological findings. Acta Neuropathol. 1994; 88(5):405-412.
24. Steele JC, McGeer PL. The ALS/PDC syndrome of Guam and the cycad hypothesis. Neurology. 2008;70(21):1984-1990.
25. Kaji R, Izumi Y, Adachi Y, Kuzuhara S. ALS-parkinsonism-dementia complex of Kii and other related diseases in Japan. Parkinsonism Relat Disord. 2012;18(suppl 1): S190-S191.
26. McGeer PL, Steele JC. The ALS/PDC syndrome of Guam: potential biomarkers for an enigmatic disorder. Prog Neurobiol. 2011;95(4):663-669.
27. Spencer P, Fry RC, Kisby GE. Unraveling 50-year-old clues linking neuro-degeneration and cancer to cycad toxins: are microRNAs common mediators? Front Genet. 2012;3:192.
28. Spencer PS, Fry RC, Palmer VS, Kisby GE. Western Pacific ALS-PDC: a prototypical neurodegenerative disorder linked to DNA damage and aberrant proteogenesis? Front Neurol. 2012;3:180.
29. Stein TD, Alvarez VE, McKee AC. Chronic traumatic encephalopathy: a spectrum of neuropathological changes following repetitive brain trauma in athletes and military personnel. Alzheimers Res Ther. 2014;6(1):4.
30. Cruts M, Theuns J, Van Broeckhoven C. Locus-specific mutation databases for neurodegenerative brain diseases. Hum Mutat. 2012;33(9):1340-1344.
31. Lehman EJ, Hein MJ, Baron SL, Gersic CM. Neurodegenerative causes of death among retired National Football League players. Neurology. 2012;79(19): 1970-1974.
32. Savica R, Parisi JE, Wold LE, Josephs KA, Ahlskog JE. High school football and risk of neurodegeneration: a community-based study. Mayo Clin Proc. 2012;87 (4):335-340.
33. Musiek ES, Schindler SE. Alzheimer disease: current concepts & future directions. Mo Med. 2013;110(5):395-400.
34. Thal DR, Rüb U, Orantes M, Braak H. Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology. 2002;58 (12):1791-1800.
35. Braak H, Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 1991;82(4):239-259.
36. Mirra SS, Heyman A, McKeel D, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropath-ologic assessment of Alzheimer's disease. Neurology. 1991;41(4):479-486.
37. Nelson PT, Alafuzoff I, Bigio EH, et al. Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J Neuropathol Exp Neurol. 2012;71(5):362-381.
38. Ghani M, Rogaeva E. Autosomal dominant Alzheimer's disease: underlying causes. In: Galimberti D, Scarpini E, eds. Neurodegenerative Diseases. London, UK: Springer-Verlag; 2014:27-47.
39. Combarros O. Genetic risk factors for Alzheimer's disease. In: Galimberti D, Scarpini E, eds. Neurodegenerative Diseases. London, UK: Springer-Verlag; 2014: 49-64.
40. Warren JD, Rohrer JD, Rossor MN. Clinical review. Frontotemporal dementia. BMJ. 2013;347:f4827.
41. Onyike CU, Diehl-Schmid J. The epidemiology of frontotemporal dementia. Int Rev Psychiatry. 2013;25(2):130-137.
42. Kirshner HS. Frontotemporal dementia and primary progressive aphasia, a review. Neuropsychiatr Dis Treat. 2014;10:1045-1055.
43. Pijnenburg YAL. New diagnostic criteria for the Behavioural variant of frontotemporal dementia. Eur Neurol Rev. 2011;6(4):234-237.
44. Perry DC, Miller BL. Frontotemporal dementia. Semin Neurol. 2013;33(4): 336-341.
45. Mackenzie IR, Neumann M, Bigio EH, et al. Nomenclature and nosology for neuropathologic subtypes of frontotemporal lobar degeneration: an update. Acta Neuropathol. 2010;119(1):1-4.
46. Urwin H, Josephs KA, Rohrer JD, et al. FUS pathology defines the majority of tau-and TDP-43-negative frontotemporal lobar degeneration. Acta Neuropathol. 2010;120(1):33-41.
47. Wood EM, Falcone D, Suh E, et al. Development and validation of pedigree classification criteria for frontotemporal lobar degeneration. JAMA Neurol. 2013; 70(11):1411-1417.
48. Serpente M, Galimberti D. Frontotemporal lobar degeneration: genetics and clinical phenotypes. In: Galimberti D, Scarpini E, eds. Neurodegenerative Diseases. London, UK: Springer-Verlag; 2014:93-109.
49. Goedert M, Spillantini MG. Pathogenesis of the tauopathies. J Mol Neurosci. 2011;45(3):425-431.
50. Lee G, Leugers CJ. Tau and tauopathies. Prog Mol Biol Transl Sci. 2012;107: 263-293.
51. Buée L, Bussière T, Buée-Scherrer V, Delacourte A, Hof PR. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev. 2000;33(1):95-130.
52. Morris M, Maeda S, Vossel K, Mucke L. The many faces of tau. Neuron. 2011;70 (3):410-426.
53. Trojanowski JQ, Schuck T, Schmidt ML, Lee VM. Distribution of tau proteins in the normal human central and peripheral nervous system. J Histochem Cytochem. 1989;37(2):209-215.
54. Shahim P, Tegner Y, Wilson DH, et al. Blood biomarkers for brain injury in concussed professional ice hockey players. JAMA Neurol. 2014;71(6):684-692.
55. Andreadis A. Tau gene alternative splicing: expression patterns, regulation and modulation of function in normal brain and neurodegenerative diseases. Biochim Biophys Acta. 2005;1739(2-3):91-103.
56. Lee VM, Goedert M, Trojanowski JQ. Neurodegenerative tauopathies. Annu Rev Neurosci. 2001;24:1121-1159.
57. Dickson DW, Kouri N, Murray ME, Josephs KA. Neuropathology of frontotemporal lobar degeneration-tau (FTLD-tau). J Mol Neurosci. 2011;45 (3):384-389.
58. Ramage SN, Anthony IC, Carnie FW, Busuttil A, Robertson R, Bell JE. Hyperphosphorylated tau and amyloid precursor protein deposition is increased in the brains of young drug abusers. Neuropathol Appl Neurobiol. 2005;31(4): 439-448.
59. Augustinack JC, Schneider A, Mandelkow EM, Hyman BT. Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. 2002;103(1):26-35.
60. Arendt T, Stieler J, Strijkstra AM, et al. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci. 2003;23(18):6972-6981.
61. Mandelkow EM, Mandelkow E. Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb Perspect Med. 2012;2(7): a006247.
62. Matsuo ES, Shin RW, Billingsley ML, et al. Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron. 1994;13(4):989-1002.
63. Corsellis JA, Bruton CJ, Freeman-Browne D. The aftermath of boxing. Psychol Med. 1973;3(3):270-303.
64. Roberts GW, Allsop D, Bruton C. The occult aftermath of boxing. J Neurol Neurosurg Psychiatry. 1990;53(5):373-378.
65. Tokuda T, Ikeda S, Yanagisawa N, Ihara Y, Glenner GG. Re-examination of ex-boxers' brains using immunohistochemistry with antibodies to amyloid beta-protein and tau protein. Acta Neuropathol. 1991;82(4):280-285.
66. Dickson DW, Farlo J, Davies P, Crystal H, Fuld P, Yen SH. Alzheimer's disease. A double-labeling immunohistochemical study of senile plaques. Am J Pathol. 1988;132(1):86-101.
67. Areza-Fegyveres R, Rosemberg S, Castro RM, et al. Dementia pugilistica with clinical features of Alzheimer's disease. Arq Neuropsiquiatr. 2007;65(3B): 830-833.
68. Schmidt ML, Zhukareva V, Newell KL, Lee VM, Trojanowski JQ. Tau isoform profile and phosphorylation state in dementia pugilistica recapitulate Alzheimer's disease. Acta Neuropathol. 2001;101(5):518-524.
69. 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(2):124-132.
70. Graham DI, Gentleman SM, Nicoll JA, et al. Altered beta-APP metabolism after head injury and its relationship to the aetiology of Alzheimer's disease. Acta Neurochir Suppl. 1996;66:96-102.
71. Montine TJ, Phelps CH, Beach TG, et al. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: a practical approach. Acta Neuropathol. 2012;123(1):1-11.
72. Hardy JA, Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science. 1992;256(5054):184-185.
73. Glenner GG, Wong CW. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun. 1984;120(3):885-890.
74. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA. 1985;82(12):4245-4249.
75. Glenner GG, Wong CW. Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun. 1984;122(3):1131-1135.
76. Arai T, Ikeda K, Akiyama H, et al. A high incidence of apolipoprotein E epsilon4 allele in middle-aged non-demented subjects with cerebral amyloid beta protein deposits. Acta Neuropathol. 1999;97(1):82-84.
77. Janssens J, Van Broeckhoven C. Pathological mechanisms underlying TDP-43 driven neurodegeneration in FTLD-ALS spectrum disorders. Hum Mol Genet. 2013;22(R1):R77-R87.
78. Wilson AC, Dugger BN, Dickson DW, Wang DS. TDP-43 in aging and Alzheimer's disease-A review. Int J Clin Exp Pathol. 2011;4(2):147-155.
79. Neumann M, Sampathu DM, Kwong LK, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 2006;314(5796):130-133.
80. Lagier-Tourenne C, Polymenidou M, Cleveland DW. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum Mol Genet. 2010;19(R1):R46-R64.
81. Buratti E, Baralle FE. TDP-43: gumming up neurons through protein-protein and protein-RNA interactions. Trends Biochem Sci. 2012;37(6):237-247.
82. Bäumer D, Talbot K, Turner MR. Advances in motor neurone disease. J R Soc Med. 2014;107(1):14-21.
83. McMillan CT, Toledo JB, Avants BB, et al. Genetic and neuroanatomic associations in sporadic frontotemporal lobar degeneration. Neurobiol Aging. 2014;35(6):1473-1482.
84. Rohrer JD, Geser F, Zhou J, et al. TDP-43 subtypes are associated with distinct atrophy patterns in frontotemporal dementia. Neurology. 2010;75(24):2204-2211.
85. Sampathu DM, Neumann M, Kwong LK, et al. Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohistochemistry and novel monoclonal antibodies. Am J Pathol. 2006;169(4):1343-1352.
86. Trojanowski JQ, Newman PD, Hill WD, Lee VM. Human olfactory epithelium in normal aging, Alzheimer's disease, and other neurodegenerative disorders. J Comp Neurol. 1991;310(3):365-376.
87. Gelber RP, Launer LJ, White LR. The Honolulu-Asia Aging Study: epidemi-ologic and neuropathologic research on cognitive impairment. Curr Alzheimer Res. 2012;9(6):664-672.
88. White L. Brain lesions at autopsy in older Japanese-American men as related to cognitive impairment and dementia in the final years of life: a summary report from the Honolulu-Asia aging study. J Alzheimers Dis. 2009;18(3): 713-725.
89. Driscoll I, Resnick SM, Troncoso JC, An Y, O'Brien R, Zonderman AB. Impact of Alzheimer's pathology on cognitive trajectories in nondemented elderly. Ann Neurol. 2006;60(6):688-695.
90. Brayne C, Richardson K, Matthews FE, et al. Neuropathological correlates of dementia in over-80-year-old brain donors from the population-based Cambridge city over-75s cohort (CC75C) study. J Alzheimers Dis. 2009;18(3): 645-658.
91. Au R, Seshadri S, Knox K, et al. The Framingham Brain Donation Program: neuropathology along the cognitive continuum. Curr Alzheimer Res. 2012;9(6): 673-686.
92. Snowdon DA, Nun S. Healthy aging and dementia: findings from the Nun Study. Ann Intern Med. 2003;139(5 pt 2):450-454.
93. Snowdon DA. Aging and Alzheimer's disease: lessons from the Nun Study. Gerontologist. 1997;37(2):150-156.
94. Sonnen JA, Larson EB, Crane PK, et al. Pathological correlates of dementia in a longitudinal, population-based sample of aging. Ann Neurol. 2007;62(4): 406-413.
95. Mortimer JA. The Nun Study: risk factors for pathology and clinical-pathologic correlations. Curr Alzheimer Res. 2012;9(6):621-627.
96. Irwin DJ, Cohen TJ, Grossman M, et al. Acetylated tau, a novel pathological signature in Alzheimer's disease and other tauopathies. Brain. 2012;135(pt 3): 807-818.
97. Irwin DJ, Cohen TJ, Grossman M, et al. Acetylated tau neuropathology in sporadic and hereditary tauopathies. Am J Pathol. 2013;183(2):344-351.
98. Lim J, Lu KP. Pinning down phosphorylated tau and tauopathies. Biochim Biophys Acta. 2005;1739(2-3):311-322.
99. Higuchi M, Trojanoswki JQ, Lee VM-Y. Tau protein and tauopathy. In: Davis KL, Charney D, Coyle JT, Nemeroff C, eds. Neuropsychopharmacology: The Fifth Generation of Progress. Philadelphia, PA: LWW; 2002:1339-1354.
100. Bugiani O, Mancardi GL, Brusa A, Ederli A. The fine structure of subcortical neurofibrillary tangles in progressive supranuclear palsy. Acta Neuropathol. 1979; 45(2):147-152.
101. Johnson GV, Stoothoff WH. Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci. 2004;117(pt 24):5721-5729.