Chronic traumatic encephalopathy: Where are we and where are we going? topical collection on dementia

Current Neurology and Neuroscience Reports

Volumn 13, Issue 12, 2013, Pages

  Mez, Jesse ^a   Stern, Robert A ^a   McKee, Ann C ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA BOSTON HEALTHCARE SYSTEM   (United States)

Author keywords

Apolipoprotein E (APOE E); Chronic traumatic encephalopathy (CTE); Concussion; Dementia pugilistica; Neurofibrillary tangle; Tauopathy; TDP 43; Traumatic brain injury (TBI)

Indexed keywords

BIOLOGICAL MARKER;

ARTICLE; CEREBROSPINAL FLUID ANALYSIS; CHRONIC TRAUMATIC ENCEPHALOPATHY; CLINICAL FEATURE; COMPUTER ASSISTED TOMOGRAPHY; DISEASE ASSOCIATION; GENETIC ASSOCIATION; HUMAN; NEUROIMAGING; NEUROPATHOLOGY; NEUROPSYCHOLOGICAL TEST; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TRAUMATIC BRAIN INJURY; ANIMAL; BOXING; BRAIN INJURY; GENETICS; INJURY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PSYCHOLOGICAL ASPECT; REVIEW;

BRAIN INJURY, CHRONIC; ANIMALS; BIOLOGICAL MARKERS; BOXING; HUMANS; MAGNETIC RESONANCE IMAGING; NEUROIMAGING; NEUROPSYCHOLOGICAL TESTS; POSITRON-EMISSION TOMOGRAPHY; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84890517232     PISSN: 15284042     EISSN: 15346293     Source Type: Journal    
DOI: 10.1007/s11910-013-0407-7     Document Type: Article

References (117)

1. • Martland HS. Punch drunk. J Am Med Assoc. 1928;91:1103-7. This is the first mention of CTE (called "punch drunk" in the text) in the medical literature.
2. Parker HL. Traumatic encephalopathy ('punch drunk') of professional pugilists. J Neurol Psychopathol. 1934;15:20-8.
3. Millspaugh J. Dementia pugilistica. US Nav Med Bull. 1937;297-303.
4. • Corsellis JA, Bruton CJ, Freeman-Browne D. The aftermath of boxing. Psychol Med. 1973;3:270-303. This landmark series of 15 cases described the clinical and pathological features that differentiate CTE (called "dementia pugilistica" in the text) from other neurodegenerative diseases.
5. Omalu BI, DeKosky ST, Hamilton RL, Minster RL, Kamboh MI, Shakir AM, et al. Chronic traumatic encephalopathy in a national football league player: part II. Neurosurgery. 2006;59:1086-92.
6. Omalu BI, DeKosky ST, Minster RL, Kamboh MI, Hamilton RL, Wecht CH. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery. 2005;57:128-34.
7. McKee AC, Cantu RC, Nowinski CJ, Hedley-Whyte ET, Gavett BE, Budson AE, et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol. 2009;68:709-35.
8. •• McKee AC, Stein TD, Nowinski CJ, Stern RA, Daneshvar DH, Alvarez VE, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain. 2013;136:43-64. This is largest modern pathologically confirmed CTE case series to date. It also lays out criteria for the pathological definition and staging of CTE.
9. Omalu B, Bailes J, Hamilton RL, Kamboh MI, Hammers J, Case M, et al. Emerging histomorphologic phenotypes of chronic traumatic encephalopathy in American athletes. Neurosurgery. 2011;69:173-83.
10. Jordan BD. The clinical spectrum of sport-related traumatic brain injury. Nat Rev Neurol. 2013;9:222-30.
11. Jordan BD. Medical aspects of boxing. CRC Press; 1993.
12. • Guskiewicz KM, Marshall SW, Bailes J, McCrea M, Cantu RC, Randolph C, et al. Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery. 2005;57:719-26. This important epidemiologic study of former professional American football players found a fivefold increase of MCI in players with a history of three or more concussions compared with players without a concussion history. It suggests that repeated concussive brain injury may be a risk factor for CTE.
13. McCrory P, Meeuwisse WH, Kutcher JS, Jordan BD, Gardner A. What is the evidence for chronic concussion-related changes in retired athletes: behavioural, pathological and clinical outcomes? Br J Sports Med. 2013;47:327-30.
14. • Goldstein LE, Fisher AM, Tagge CA, Zhang X-L, Velisek L, Sullivan JA, et al. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci Transl Med. 2012;4:134-60. In this study, pathology in some ways analogous to CTE was identified in wild-type mice 2 weeks after a controlled blast exposure. The study supplies evidence for the relationship between mTBI and CTE, and also provides a mouse model for future CTE research.
15. Mouzon B, Chaytow H, Crynen G, Bachmeier C, Stewart J, Mullan M, et al. Repetitive mild traumatic brain injury in a mouse model produces learning and memory deficits accompanied by histological changes. J Neurotrauma. 2012;29:2761-73.
16. Ojo J-O, Mouzon B, Greenberg MB, Bachmeier C, Mullan M, Crawford F. Repetitive mild traumatic brain injury augments tau pathology and glial activation in aged hTau mice. J Neuropathol Exp Neurol. 2013;72:137-51.
17. Giza CC, Kutcher JS, Ashwal S, Barth J, Getchius TSD, Gioia GA, 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;80:2250-7.
18. International Statistical Classification of Diseases and Related Health Problems 10th Revision (ICD-10) Version for 2010, F07.2 Postconcussional syndrome. World Health Organization.
19. American Psychiatric Association. Diagnostic and statistical manual of mental disorders DSM-IV-TR fourth edition. American Psychiatric Publishing; 2000.
20. Jotwani V, Harmon KG. Postconcussion syndrome in athletes. Curr Sports Med Rep. 2010;9:21-6.
21. Crisco JJ, Wilcox BJ, Beckwith JG, Chu JJ, Duhaime A-C, Rowson S, et al. Head impact exposure in collegiate football players. J Biomech. 2011;44:2673-8.
22. King NS, Kirwilliam S. Permanent post-concussion symptoms after mild head injury. Brain Inj. 2011;25:462-70.
23. Casson IR, Siegel O, Sham R, Campbell EA, Tarlau M, DiDomenico A. Brain damage in modern boxers. JAMA. 1984;251:2663-7.
24. Roberts AH. Brain damage in boxers; A study of the prevalence of traumatic encephalopathy among ex-professional boxers. Pitman Medical & Scientific Publishing; 1969.
25. Critchley M. Medical aspects of boxing, particularly from a neurological standpoint. Br Med J. 1957;1:357.
26. Stern RA, Daneshvar DH, Baugh CM, Seichepine DR, Montenigro BS, Riley DO, et al. Clinical presentation of chronic traumatic encephalopathy. Neurology. 2013;81:1122-9.
27. •• McKee AC, Gavett BE, Stern RA, Nowinski CJ, Cantu RC, Kowall NW, et al. TDP-43 proteinopathy and motor neuron disease in chronic traumatic encephalopathy. J Neuropathol Exp Neurol. 2010;69:918-29. This is the first study to provide evidence for an association between CTE and MND.
28. Mawdsley C, Ferguson FR. Neurological disease in boxers. Lancet. 1963;2:799-801.
29. Gavett BE, Cantu RC, Shenton M, Lin AP, Nowinski CJ, McKee AC, et al. Clinical appraisal of chronic traumatic encephalopathy: current perspectives and future directions. Curr Opin Neurol. 2011;24:525-31.
30. Ferrari R, Kapogiannis D, Huey ED, Momeni P. FTD and ALS: a tale of two diseases. Curr Alzheimer Res. 2011;8:273-94.
31. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Neuhaus J, et al. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain J Neurol. 2011;134:2456-77.
32. Hanson JC, Lippa CF. Chapter 11 Lewy body dementia. Int Rev Neurobiol. 2009;84:215-28.
33. Hof PR, Knabe R, Bovier P, Bouras C. Neuropathological observations in a case of autism presenting with self-injury behavior. Acta Neuropathol (Berl). 1991;82:321-6.
34. Hazrati L-N, Tartaglia MC, Diamandis P, Davis KD, Green RE, Wennberg R, et al. Absence of chronic traumatic encephalopathy in retired football players with multiple concussions and neurological symptomatology. Front Hum Neurosci. 2013;7:222.
35. 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;31:130-2.
36. 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 (Berl). 2001;101:518-24.
37. Geddes JF, Vowles GH, Nicoll JA, Révész T. Neuronal cytoskeletal changes are an early consequence of repetitive head injury. Acta Neuropathol (Berl). 1999;98:171-8.
38. Roberts GW, Whitwell HL, Acland PR, Bruton CJ. Dementia in a punch-drunk wife. Lancet. 1990;335:918-9.
39. Hof PR, Bouras C, Buée L, Delacourte A, Perl DP, Morrison JH. Differential distribution of neurofibrillary tangles in the cerebral cortex of dementia pugilistica and Alzheimer's disease cases. Acta Neuropathol (Berl). 1992;85:23-30.
40. Sivanandam TM, Thakur MK. Traumatic brain injury: a risk factor for Alzheimer's disease. Neurosci Biobehav Rev. 2012;36:1376-81.
41. Goldman SM, Tanner CM, Oakes D, Bhudhikanok GS, Gupta A, Langston JW. Head injury and Parkinson's disease risk in twins. Ann Neurol. 2006;60:65-72.
42. Schmidt S, Kwee LC, Allen KD, Oddone EZ. Association of ALS with head injury, cigarette smoking and APOE genotypes. J Neurol Sci. 2010;291:22-9.
43. Pupillo E, Messina P, Logroscino G, Zoccolella S, Chiò A, Calvo A, et al. Trauma and amyotrophic lateral sclerosis: a case-control study from a population-based registry. Eur J Neurol. 2012;19:1509-17.
44. Johnson VE, Stewart W, Smith DH. Axonal pathology in traumatic brain injury. Exp Neurol. 2013;246:35-43.
45. Jordan BD, Matser EJ, Zimmerman RD, Zazula T. Sparring and cognitive function in professional boxers. Phys Sportsmed. 1996;24:87-98.
46. Jordan BD, Jahre C, Hauser WA, Zimmerman RD, Zarrelli M, Lipsitz EC, et al. CT of 338 active professional boxers. Radiology. 1992;185:509-12.
47. Clausen H, McCrory P, Anderson V. The risk of chronic traumatic brain injury in professional boxing: change in exposure variables over the past century. Br J Sports Med. 2005;39:661-4.
48. Guskiewicz KM, Marshall SW, Bailes J, McCrea M, Harding Jr HP, Matthews A, et al. Recurrent concussion and risk of depression in retired professional football players. Med Sci Sports Exerc. 2007;39:903-9.
49. • Lehman EJ, Hein MJ, Baron SL, Gersic CM. Neurodegenerative causes of death among retired National Football League players. Neurology. 2012;79:1970-4. This recent epidemiological study of professional American football players demonstrated a threefold increase in neurodegenerative death compared with the general population. While mortality from CTE could not be examined as it is not listed as a cause of death in the International Classification of Diseases, at least some of the neurodegenerative deaths were presumably due to CTE.
50. Loosemore M, Knowles CH, Whyte GP. Amateur boxing and risk of chronic traumatic brain injury: systematic review of observational studies. Br J Sports Med. 2008;42:564-7.
51. Savica R, Parisi JE, Wold LE, Josephs KA, Ahlskog JE. High school football and risk of neurodegeneration: a community-based study. Mayo Clin Proc Mayo Clin. 2012;87:335-40.
52. Mannix R, O'Brien MJ, Meehan 3rd WP. The epidemiology of outpatient visits for minor head injury 2005-2009. Neurosurgery. 2013;73:129-34.
53. Management of Concussion/mTBI Working Group. VA/DoD clinical practice guideline for management of concussion/mild traumatic brain injury. J Rehabil Res Dev. 2009;46:CP1-CP68.
54. Faul M, Xu L, Wald MM, Coronado VG. Traumatic brain injury in the United States: Emergency department visits, hospitalizations and deaths 2002-2006. Center for Disease Control and Prevention; 2010.
55. Zemper ED. Two-year prospective study of relative risk of a second cerebral concussion. Am J Phys Med Rehabil. 2003;82:653-9.
56. Guskiewicz KM, McCrea M, Marshall SW, Cantu RC, Randolph C, Barr W, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA. 2003;290:2549-55.
57. Schneider GE. Is it really better to have your brain lesion early? A revision of the "Kennard principle". Neuropsychologia. 1979;17:557-83.
58. Stern RA, Riley DO, Daneshvar DH, Nowinski CJ, Cantu RC, McKee AC. Long-term consequences of repetitive brain trauma: chronic traumatic encephalopathy. PM R. 2011;3(10 Suppl 3):S460-7.
59. Zemek RL, Farion KJ, Sampson M, McGahern C. Prognosticators of persistent symptoms following pediatric concussion: a systematic review. JAMA Pediatr. 2013;167:259-65.
60. Field M, Collins MW, Lovell MR, Maroon J. Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J Pediatr. 2003;142:546-53.
61. Vagnozzi R, Signoretti S, Cristofori L, Alessandrini F, Floris R, Isgrò E, 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 J Neurol. 2010;133:3232-42.
62. Maugans TA, Farley C, Altaye M, Leach J, Cecil KM. Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics. 2012;129:28-37.
63. Colvin AC, Mullen J, Lovell MR, West RV, Collins MW, Groh M. The role of concussion history and gender in recovery from soccer-related concussion. Am J Sports Med. 2009;37:1699-704.
64. Broshek DK, Kaushik T, Freeman JR, Erlanger D, Webbe F, Barth JT. Sex differences in outcome following sports-related concussion. J Neurosurg. 2005;102:856-63.
65. Covassin T, Schatz P, Swanik CB. Sex differences in neuropsychological function and post-concussion symptoms of concussed collegiate athletes. Neurosurgery. 2007;61:345-50.
66. Dick RW. Is there a gender difference in concussion incidence and outcomes? Br J Sports Med. 2009;43 Suppl 1:i46-50.
67. Mayeux R, Ottman R, Maestre G, Ngai C, Tang MX, Ginsberg H, et al. Synergistic effects of traumatic head injury and apolipoprotein-epsilon 4 in patients with Alzheimer's disease. Neurology. 1995;45:555-7.
68. 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.
69. Jellinger KA, Paulus W, Wrocklage C, Litvan I. Effects of closed traumatic brain injury and genetic factors on the development of Alzheimer's disease. Eur J Neurol. 2001;8:707-10.
70. Jordan BD, Relkin NR, Ravdin LD, Jacobs AR, Bennett A, Gandy S. Apolipoprotein E epsilon4 associated with chronic traumatic brain injury in boxing. JAMA. 1997;278:136-40.
71. Kutner KC, Erlanger DM, Tsai J, Jordan B, Relkin NR. Lower cognitive performance of older football players possessing apolipoprotein E epsilon4. Neurosurgery. 2000;47:651-7.
72. Crawford F, Wood M, Ferguson S, Mathura V, Gupta P, Humphrey J, et al. Apolipoprotein E-genotype dependent hippocampal and cortical responses to traumatic brain injury. Neuroscience. 2009;159:1349-62.
73. Mahley RW, Huang Y. Apolipoprotein e sets the stage: response to injury triggers neuropathology. Neuron. 2012;76:871-85.
74. • Belanger HG, Spiegel E, Vanderploeg RD. Neuropsychological performance following a history of multiple self-reported concussions: a meta-analysis. J Int Neuropsychol Soc. 2010;16:262-7. This meta-analysis of eight studies of healthy former athletes found that a history of two or more concussions was associated with reduced delayed recall and executive function compared with a history of only one concussion. It provides evidence for poorer outcomes from repeated versus single brain trauma and suggests a possible neuropsychological profile for CTE.
75. • Talavage TM, Nauman EA, Breedlove EL, Yoruk U, Dye AE, Morigaki KE, et al. Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J Neurotrauma. 2013 Apr 11 [Epub ahead of print]. This recent study of high school football players who did not report any cognitive symptoms over the course of a season found lower scores in visual working memory and decreased activation in the dorsolateral frontal cortex on fMRI on post-season evaluation compared with pre-season evaluation. It provides neuropsychological and imaging evidence for subconcussive injury.
76. • Hart J Jr, Kraut MA, Womack KB, Strain J, Didehbani N, Bartz E, et al. Neuroimaging of cognitive dysfunction and depression in aging retired National Football League players: a cross-sectional study. JAMA Neurol. 2013;70:326-35. This recent study of retired professional American football players, about half of whom had cognitive impairment, described the neuropsychological profile of the impairment and found differences on MRI DTI and ASL in the impaired players compared with controls. This study provides some of the first imaging and neuropsychological testing data in patients with presumed CTE.
77. Ross RJ, Cole M, Thompson JS, Kim KH. Boxers - computed tomography, EEG, and neurological evaluation. JAMA. 1983;249:211-3.
78. MacKenzie JD, Siddiqi F, Babb JS, Bagley LJ, Mannon LJ, Sinson GP, et al. Brain atrophy in mild or moderate traumatic brain injury: a longitudinal quantitative analysis. AJNR Am J Neuroradiol. 2002;23:1509-15.
79. Toth A, Kovacs N, Perlaki G, Orsi G, Aradi M, Komaromy H, et al. Multi-modal magnetic resonance imaging in the acute and sub-acute phase of mild traumatic brain injury: can we see the difference? J Neurotrauma. 2013;30:2-10.
80. Zhou Y, Kierans A, Kenul D, Ge Y, Rath J, Reaume J, et al. Mild traumatic brain injury: longitudinal regional brain volume changes. Radiology. 2013;267:880-90.
81. Scheid R, Preul C, Gruber O, Wiggins C, von Cramon DY. Diffuse axonal injury associated with chronic traumatic brain injury: evidence from T2-weighted gradient-echo imaging at 3 T. AJNR Am J Neuroradiol. 2003;24:1049-56.
82. Hähnel S, Stippich C, Weber I, Darm H, Schill T, Jost J, et al. Prevalence of cerebral microhemorrhages in amateur boxers as detected by 3 T MR imaging. AJNR Am J Neuroradiol. 2008;29:388-91.
83. Hasiloglu ZI, Albayram S, Selcuk H, Ceyhan E, Delil S, Arkan B, et al. Cerebral microhemorrhages detected by susceptibility-weighted imaging in amateur boxers. AJNR Am J Neuroradiol. 2011;32:99-102.
84. Park J-H, Park S-W, Kang S-H, Nam T-K, Min B-K, Hwang S-N. Detection of traumatic cerebral microbleeds by susceptibility-weighted image of MRI. J Korean Neurosurg Soc. 2009;46:365-9.
85. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging JMRI. 2001;13:534-46.
86. Aoki Y, Inokuchi R, Gunshin M, Yahagi N, Suwa H. Diffusion tensor imaging studies of mild traumatic brain injury: a meta-analysis. J Neurol Neurosurg Psychiatry. 2012;83:870-6.
87. Arfanakis K, Haughton VM, Carew JD, Rogers BP, Dempsey RJ, Meyerand ME. Diffusion tensor MR imaging in diffuse axonal injury. AJNR Am J Neuroradiol. 2002;23:794-802.
88. Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips JP, Doezema D, et al. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology. 2010;74:643-50.
89. Grossman EJ, Jensen JH, Babb JS, Chen Q, Tabesh A, Fieremans E, et al. Cognitive impairment in mild traumatic brain injury: a longitudinal diffusional kurtosis and perfusion imaging study. Am J Neuroradiol. 2013;34:951-7.
90. Messé A, Caplain S, Paradot G, Garrigue D, Mineo J-F, Soto Ares G, et al. Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairment. Hum Brain Mapp. 2011;32:999-1011.
91. Koerte IK, Kaufmann D, Hartl E, Bouix S, Pasternak O, Kubicki M, et al. A prospective study of physician-observed concussion during a varsity university hockey season: white matter integrity in ice hockey players. Part 3 of 4. Neurosurg Focus. 2012;33(E3):1-7.
92. • Koerte IK, Ertl-Wagner B, Reiser M, Zafonte R, Shenton ME. White matter integrity in the brains of professional soccer players without a symptomatic concussion. JAMA. 2012;308:1859-61. This study of professional soccer players who had never suffered a concussion found evidence of white matter injury suggestive of repeated mTBI on MRI DTI, providing evidence for subconcussive injury.
93. Radanovic M, Pereira FRS, Stella F, Aprahamian I, Ferreira LK, Forlenza OV, et al. White matter abnormalities associated with Alzheimer's disease and mild cognitive impairment: a critical review of MRI studies. Expert Rev Neurother. 2013;13:483-93.
94. Amaro Jr E, Barker GJ. Study design in fMRI: basic principles. Brain Cogn. 2006;60:220-32.
95. Bryer EJ, Medaglia JD, Rostami S, Hillary FG. Neural recruitment after mild traumatic brain injury is task dependent: a meta-analysis. J Int Neuropsychol Soc. 2013;19:751-62.
96. Johnson B, Zhang K, Gay M, Horovitz S, Hallett M, Sebastianelli W, et al. Alteration of brain default network in subacute phase of injury in concussed individuals: resting-state fMRI study. Neuroimage. 2012;59:511-8.
97. Zhou Y, Milham MP, Lui YW, Miles L, Reaume J, Sodickson DK, et al. Default-mode network disruption in mild traumatic brain injury. Radiology. 2012;265:882-92.
98. Mayer AR, Mannell MV, Ling J, Gasparovic C, Yeo RA. Functional connectivity in mild traumatic brain injury. Hum Brain Mapp. 2011;32:1825-35.
99. Wolk DA, Detre JA. Arterial Spin Labeling MRI: An emerging biomarker for Alzheimer's disease and other neurodegenerative conditions. Curr Opin Neurol. 2012;25:421-8.
100. Lin AP, Liao HJ, Merugumala SK, Prabhu SP, Meehan 3rd WP, Ross BD. Metabolic imaging of mild traumatic brain injury. Brain Imaging Behav. 2012;6:208-23.
101. Vagnozzi R, Signoretti S, Tavazzi B, Floris R, Ludovici A, Marziali S, et al. Temporal window of metabolic brain vulnerability to concussion: a pilot 1H-magnetic resonance spectroscopic study in concussed athletes - part III. Neurosurgery. 2008;62:1286-95.
102. Henry LC, Tremblay S, Leclerc S, Khiat A, Boulanger Y, Ellemberg D, et al. Metabolic changes in concussed American football players during the acute and chronic post-injury phases. BMC Neurol. 2011;11:105.
103. Yeo RA, Gasparovic C, Merideth F, Ruhl D, Doezema D, Mayer AR. A longitudinal proton magnetic resonance spectroscopy study of mild traumatic brain injury. J Neurotrauma. 2011;28:1-11.
104. Warwick JM. Imaging of brain function using SPECT. Metab Brain Dis. 2004;19:113-23.
105. Audenaert K, Jansen HML, Otte A, Peremans K, Vervaet M, Crombez R, et al. Imaging of mild traumatic brain injury using 57Co and 99mTc HMPAO SPECT as compared to other diagnostic procedures. Med Sci Monit Int Med J Exp Clin Res. 2003;9:MT112-7.
106. Amen DG, Newberg A, Thatcher R, Jin Y, Wu J, Keator D, et al. Impact of playing American professional football on long-term brain function. J Neuropsychiatry Clin Neurosci. 2011;23:98-106.
107. Jacobs A, Put E, Ingels M, Put T, Bossuyt A. One-year follow-up of technetium-99 m-HMPAO SPECT in mild head injury. J Nucl Med. 1996;37:1605-9.
108. Singhal T. Positron emission tomography applications in clinical neurology. Semin Neurol. 2012;32:421-31.
109. Provenzano FA, Jordan B, Tikofsky RS, Saxena C, Van Heertum RL, Ichise M. F-18 FDG PET imaging of chronic traumatic brain injury in boxers: a statistical parametric analysis. Nucl Med Commun. 2010;31:952-7.
110. Peskind ER, Petrie EC, Cross DJ, Pagulayan K, McCraw K, Hoff D, 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:S76-82.
111. Chien DT, Bahri S, Szardenings AK, Walsh JC, Mu F, Su M-Y, et al. Early clinical PET imaging results with the novel PHF-tau radioligand [F-18]-T807. J Alzheimers Dis. 2013;34:457-68.
112. Small GW, Kepe V, Siddarth P, Ercoli LM, Merrill DA, Donoghue N, et al. PET Scanning of Brain Tau in Retired National Football League Players: Preliminary Findings. Am J Geriatr Psychiatry. 2013;21:138-44.
113. Zetterberg H, Hietala MA, Jonsson M, Andreasen N, Styrud E, Karlsson I, et al. Neurochemical aftermath of amateur boxing. Arch Neurol. 2006;63:1277-80.
114. Neselius S, Brisby H, Theodorsson A, Blennow K, Zetterberg H, Marcusson J. CSF-biomarkers in Olympic boxing: diagnosis and effects of repetitive head trauma. PloS One. 2012;7:e33606.
115. Zetterberg H, Smith DH, Blennow K. Biomarkers of mild traumatic brain injury in cerebrospinal fluid and blood. Nat Rev Neurol. 2013;9:201-10.
116. Metting Z, Wilczak N, Rodiger LA, Schaaf JM, van der Naalt J. GFAP and S100B in the acute phase of mild traumatic brain injury. Neurology. 2012;78:1428-33.
117. Neselius S, Zetterberg H, Blennow K, Randall J, Wilson D, Marcusson J, et al. Olympic boxing is associated with elevated levels of the neuronal protein tau in plasma. Brain Inj. 2013;27:425-33.