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Mixed pathologies including chronic traumatic encephalopathy account for dementia in retired association football (soccer) players
Open accessAbstract
In retired professional association football (soccer) players with a past history of repetitive head impacts, chronic traumatic encephalopathy (CTE) is a potential neurodegenerative cause of dementia and motor impairments. From 1980 to 2010, 14 retired footballers with dementia were followed up regularly until death. Their clinical data, playing career, and concussion history were prospectively collected. Next-of-kin provided consent for six to have post-mortem brain examination. Of the 14 male participants, 13 were professional and 1 was a committed amateur. All were skilled headers of the ball and had played football for an average of 26 years. Concussion rate was limited in six cases to one episode each during their careers. All cases developed progressive cognitive impairment with an average age at onset of 63.6 years and disease duration of 10 years. Neuropathological examination revealed septal abnormalities in all six post-mortem cases, supportive of a history of chronic repetitive head impacts. Four cases had pathologically confirmed CTE; concomitant pathologies included Alzheimer's disease (N = 6), TDP-43 (N = 6), cerebral amyloid angiopathy (N = 5), hippocampal sclerosis (N = 2), corticobasal degeneration (N = 1), dementia with Lewy bodies (N = 1), and vascular pathology (N = 1); and all would have contributed synergistically to the clinical manifestations. The pathological diagnosis of CTE was established in four individuals according to the latest consensus diagnostic criteria. This finding is probably related to their past prolonged exposure to repetitive head impacts from head-to-player collisions and heading the ball thousands of time throughout their careers. Alzheimer's disease and TDP-43 pathologies are common concomitant findings in CTE, both of which are increasingly considered as part of the CTE pathological entity in older individuals. Association football is the most popular sport in the world and the potential link between repetitive head impacts from playing football and CTE as indicated from our findings is of considerable public health interest. Clearly, a definitive link cannot be established in this clinico-pathological series, but our findings support the need for further systematic investigation, including large-scale case-control studies to identify at risk groups of footballers which will justify for the implementation of protective strategies.
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“It is now well established that a large percentage of former athletes identified as having CTE neuropathology also have neuropathology associated with age related neurodegenerative diseases such as AD, PD, Lewy body disease, hippocampal sclerosis, and ALS [14, 41–44] to the extent that they meet full neuropathological criteria for an alternative, well-characterized neurodegenerative disease [16].”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [44]
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Citations
Cites
Neuropathological stageing of Alzheimer-related changes.
Braak, H., & Braak, E. (1991) · Acta Neuropathologica · doi:10.1007/bf00308809 · Cited by 16,123
Staging of brain pathology related to sporadic Parkinson’s disease
Braak, H., Tredici, K. D., Rüb, U., de Vos, R. A. I., Jansen Steur, E. N. H., & Braak, E. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00065-9 · Cited by 10,777
Diagnosis and management of dementia with Lewy bodies: Third report of the DLB consortium
McKeith, I. G., Dickson, D. W., Lowe, J., Emre, M., O'Brien, J. T., Feldman, H., Cummings, J., Duda, J. E., Lippa, C., Perry, E. K., et al. (2005) · Neurology · doi:10.1212/01.wnl.0000187889.17253.b1 · Cited by 5,069
Self-citationPhases of Aβ-deposition in the human brain and its relevance for the development of AD
Thal, D. R., Rüb, U., Orantes, M., & Braak, H. (2002) · Neurology · doi:10.1212/wnl.58.12.1791 · Cited by 3,490
Hyman, B. T., Phelps, C. H., Beach, T. G., Bigio, E. H., Cairns, N. J., Carrillo, M. C., Dickson, D. W., Duyckaerts, C., Frosch, M. P., Masliah, E., et al. (2012) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.10.007 · Cited by 3,092
Montine, T. J., Phelps, C. H., Beach, T. G., Bigio, E. H., Cairns, N. J., Dickson, D. W., Duyckaerts, C., Frosch, M. P., Masliah, E., Mirra, S. S., et al. (2012) · Acta Neuropathologica · doi:10.1007/s00401-011-0910-3 · Cited by 2,894
The spectrum of disease in chronic traumatic encephalopathy
McKee, A. C., Stein, T. D., Nowinski, C. J., Stern, R. A., Daneshvar, D. H., Alvarez, V. E., Lee, H.-S., Hall, G., Wojtowicz, S. M., Baugh, C. M., et al. (2013) · Brain · doi:10.1093/brain/aws307 · Cited by 2,098
Primary age-related tauopathy (PART): a common pathology associated with human aging
Crary, J. F., Trojanowski, J. Q., Schneider, J. A., Abisambra, J. F., Abner, E. L., Alafuzoff, I., Arnold, S. E., Attems, J., Beach, T. G., Bigio, E. H., et al. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1349-0 · Cited by 1,467
Axonal pathology in traumatic brain injury
Johnson, V. E., Stewart, W., & Smith, D. H. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2012.01.013 · Cited by 1,273
A harmonized classification system for FTLD-TDP pathology
Mackenzie, I. R., Neumann, M., Baborie, A., Sampathu, D. M., du Plessis, D., Jaros, E., Perry, R. H., Trojanowski, J. Q., Mann, D. M. A., & Lee, V. M. ‐. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0845-8 · Cited by 1,042
TDP‐43 immunoreactivity in hippocampal sclerosis and Alzheimer's disease
Amador‐Ortiz, C., Lin, W., Ahmed, Z., Personett, D., Davies, P., Duara, R., Graff‐Radford, N. R., Hutton, M. L., & Dickson, D. W. (2007) · Annals of Neurology · doi:10.1002/ana.21154 · Cited by 916
the TBI/CTE group, McKee, A. C., Cairns, N. J., Dickson, D. W., Folkerth, R. D., Dirk Keene, C., Litvan, I., Perl, D. P., Stein, T. D., Vonsattel, J.-P., et al. (2016) · Acta Neuropathologica · doi:10.1007/s00401-015-1515-z · Cited by 885
Corsellis, J. A. N., Bruton, C. J., & Freeman-Browne, D. (1973) · Psychological Medicine · doi:10.1017/s0033291700049588 · Cited by 836
Office of Rare Diseases Neuropathologic Criteria for Corticobasal Degeneration
Dickson, D. W., Bergeron, C., Chin, S. S., Duyckaerts, C., Horoupian, D., Ikeda, K., Jellinger, K., Lantos, P. L., Lippa, C. F., Mirra, S. S., et al. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.11.935 · Cited by 724
Clinical presentation of chronic traumatic encephalopathy
Stern, R. A., Daneshvar, D. H., Baugh, C. M., Seichepine, D. R., Montenigro, P. H., Riley, D. O., Fritts, N. G., Stamm, J. M., Robbins, C. A., McHale, L., et al. (2013) · Neurology · doi:10.1212/wnl.0b013e3182a55f7f · Cited by 564
Aging-related tau astrogliopathy (ARTAG): Harmonized evaluation strategy
Kovacs, G. G., Ferrer, I., Grinberg, L. T., Alafuzoff, I., Attems, J., Budka, H., Cairns, N. J., Crary, J. F., Duyckaerts, C., Ghetti, B., et al. (2016) · Acta Neuropathologica · doi:10.1007/s00401-015-1509-x · Cited by 532 · cited 3×
“1 3 (PART) [10], and age-related tau astrogliopathy (ARTAG) [23].”
Staging of Argyrophilic Grains: An Age-Associated Tauopathy
Saito, Y., Ruberu, N. N., Sawabe, M., Arai, T., Tanaka, N., Kakuta, Y., Yamanouchi, H., & Murayama, S. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.9.911 · Cited by 444
McKee, A. C., Daneshvar, D. H., Alvarez, V. E., & Stein, T. D. (2014) · Acta Neuropathologica · doi:10.1007/s00401-013-1230-6 · Cited by 422
Updated TDP-43 in Alzheimer’s disease staging scheme
Josephs, K. A., Murray, M. E., Whitwell, J. L., Tosakulwong, N., Weigand, S. D., Petrucelli, L., Liesinger, A. M., Petersen, R. C., Parisi, J. E., & Dickson, D. W. (2016) · Acta Neuropathologica · doi:10.1007/s00401-016-1537-1 · Cited by 382
Soccer Heading Is Associated with White Matter Microstructural and Cognitive Abnormalities
Lipton, M. L., Kim, N., Zimmerman, M. E., Kim, M., Stewart, W. F., Branch, C. A., & Lipton, R. B. (2013) · Radiology · doi:10.1148/radiol.13130545 · Cited by 376 · cited 2×
“The assumption is that the lighter synthetic ball may also put modern footballers at risk of subconcussion and CTE is supported by the radiological findings of abnormal white matter microstructure in young footballers who headed the ball frequently [26] and the post-mortem finding of CTE in a 29-year-old footballer wi…”
BackgroundChronic traumatic encephalopathy pathology in a neurodegenerative disorders brain bank
Bieniek, K. F., Ross, O. A., Cormier, K. A., Walton, R. L., Soto-Ortolaza, A., Johnston, A. E., DeSaro, P., Boylan, K. B., Graff-Radford, N. R., Wszolek, Z. K., et al. (2015) · Acta Neuropathologica · doi:10.1007/s00401-015-1502-4 · Cited by 323
Neuronal cytoskeletal changes are an early consequence of repetitive head injury
Geddes, J. F., Vowles, G. H., Nicoll, J. A. R., & Révész, T. (1999) · Acta Neuropathologica · doi:10.1007/s004010051066 · Cited by 323
Chronic traumatic brain injury in professional soccer players
Matser, J. T., Kessels, A. G. H., Jordan, B. D., Lezak, M. D., & Troost, J. (1998) · Neurology · doi:10.1212/wnl.51.3.791 · Cited by 319
Beta-amyloid deposition in chronic traumatic encephalopathy
Stein, T. D., Montenigro, P. H., Alvarez, V. E., Xia, W., Crary, J. F., Tripodis, Y., Daneshvar, D. H., Mez, J., Solomon, T., Meng, G., et al. (2015) · Acta Neuropathologica · doi:10.1007/s00401-015-1435-y · Cited by 291
Age of first exposure to football and later-life cognitive impairment in former NFL players
Stamm, J. M., Bourlas, A. P., Baugh, C. M., Fritts, N. G., Daneshvar, D. H., Martin, B. M., McClean, M. D., Tripodis, Y., & Stern, R. A. (2015) · Neurology · doi:10.1212/wnl.0000000000001358 · Cited by 278
White Matter Integrity in the Brains of Professional Soccer Players Without a Symptomatic Concussion
Koerte, I. K., Ertl-Wagner, B. B., Reiser, M. F., ZAFONTE, R. D., & Shenton, M. E. (2012) · JAMA · doi:10.1001/jama.2012.13735 · Cited by 245
Concussion History in Elite Male and Female Soccer Players
Barnes, B. C., Cooper, L., Kirkendall, D. T., McDermott, T., Jordan, B. D., & Garrett, W. E. J. (1998) · The American Journal of Sports Medicine · doi:10.1177/03635465980260031601 · Cited by 238
Hof, P. R., Bouras, C., Bu�e, L., Delacourte, A., Perl, D. P., & Morrison, J. H. (1992) · Acta Neuropathologica · doi:10.1007/bf00304630 · Cited by 213
Concussion Incidence in Elite College Soccer Players
Boden, B. P., Kirkendall, D. T., & Garrett, W. E. J. (1998) · The American Journal of Sports Medicine · doi:10.1177/03635465980260021301 · Cited by 208
Tysvaer, A., & Løchen, E. A. (1991) · The American Journal of Sports Medicine · doi:10.1177/036354659101900109 · Cited by 203
Neurological consequences of traumatic brain injuries in sports
Ling, H., Hardy, J., & Zetterberg, H. (2015) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2015.03.012 · Cited by 197
Self-citationMixed Brain Pathologies in Dementia: The BrainNet Europe Consortium Experience
Kovacs, G. G., Alafuzoff, I., Al-Sarraj, S., Arzberger, T., Bogdanovic, N., Capellari, S., Ferrer, I., Gelpi, E., Kövari, V., Kretzschmar, H., et al. (2008) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000161560 · Cited by 186
ALS in Italian professional soccer players: The risk is still present and could be soccer-specific
Chiò, A., Calvo, A., Dossena, M., Ghiglione, P., Mutani, R., & Mora, G. (2009) · Amyotrophic Lateral Sclerosis · doi:10.1080/17482960902721634 · Cited by 180
Concussion in chronic traumatic encephalopathy
Stein, T. D., Alvarez, V. E., & McKee, A. C. (2015) · Current Pain and Headache Reports · doi:10.1007/s11916-015-0522-z · Cited by 177
Altered Neurochemistry in Former Professional Soccer Players without a History of Concussion
Koerte, I. K., Lin, A. P., Muehlmann, M., Merugumala, S. K., Liao, H. V., Starr, T. C., Kaufmann, D., Mayinger, M. C., Steffinger, D., Fisch, B., et al. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2014.3715 · Cited by 173
Heading and Head Injuries in Soccer
Kirkendall, D. T., Jordan, S. E., & Garrett, W. E. J. (2001) · Sports Medicine · doi:10.2165/00007256-200131050-00006 · Cited by 142
Spiotta, A. M., Bartsch, A., & Benzel, E. C. (2011) · Neurosurgery · doi:10.1227/neu.0b013e31823021b2 · Cited by 107
Ling, H., Holton, J. L., Shaw, K., Davey, K., Lashley, T., & Revesz, T. (2015) · Acta Neuropathologica · doi:10.1007/s00401-015-1496-y · Cited by 106
Self-citationZhang, M. R., Red, S. D., Lin, A. H., Patel, S. S., & Sereno, A. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057364 · Cited by 89
Biomechanics of Heading a Soccer Ball: Implications for Player Safety
Babbs, C. F. (2001) · The Scientific World JOURNAL · doi:10.1100/tsw.2001.56 · Cited by 79
Chronic Traumatic Encephalopathy Presenting as Alzheimer’s Disease in a Retired Soccer Player
Grinberg, L. T., Anghinah, R., Nascimento, C. F., Amaro, E., Leite, R. P., Martin, M. D. G. M., Naslavsky, M. S., Takada, L. T., Filho, W. J., Pasqualucci, C. A., et al. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160312 · Cited by 59
Late-stage CTE pathology in a retired soccer player with dementia
Hales, C. M., Neill, S. G., Gearing, M., Cooper, D., Glass, J., & Lah, J. J. (2014) · Neurology · doi:10.1212/wnl.0000000000001081 · Cited by 46
Cavum septi pellucidi—a reason to ban boxers?: Table 1
McCrory, P. R. (2002) · British Journal of Sports Medicine · doi:10.1136/bjsm.36.3.157-a · Cited by 24
McCrory, P. R. (2002) · British Journal of Sports Medicine · doi:10.1136/bjsm.36.3.157 · Cited by 19
Xue, A. S., & Hollier, L. H. (2013) · Journal of Craniofacial Surgery · doi:10.1097/scs.0b013e3182710444 · Cited by 7
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Limbic-predominant age-related TDP-43 encephalopathy (LATE): consensus working group report
Nelson, P. T., Dickson, D. W., Trojanowski, J. Q., Jack, C. R., Boyle, P. A., Arfanakis, K., Rademakers, R., Alafuzoff, I., Attems, J., Brayne, C., et al. (2019) · Brain · doi:10.1093/brain/awz099 · Cited by 1,547
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Metadata
- Authors
- Ling, H., Morris, H. R., Neal, J. W., Lees, A. J., Hardy, J., Holton, J. L., Revesz, T., & Williams, D. D. R.
- Affiliations
- National Hospital for Neurology and Neurosurgery (GB)
- UCL Queen Square Institute of Neurology (GB)
- Cardiff University (GB)
- Cefn Coed Hospital (GB)
- Corresponding author
- Holton, Janice L.
- Venue
- Acta Neuropathologica
- Published
- 2017-02-15
- Volume
- 133
- Issue
- 3
- Pages
- 337-352
- ISSN
- 0001-6322 (ISSN-L)
- 1432-0533
- PMC
- PMC5325836
- OpenAlex
- W2588072485
- Cited by
- 252
- References
- 45
- Citations by year
- 2026: 10 · 2025: 22 · 2024: 20 · 2023: 31 · 2022: 28 · 2021: 30 · 2020: 51 · 2019: 28 · 2018: 16 · 2017: 16
- FWCI
- 23.78
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Acta Neuropathologica (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Funders
- The Drake Foundation
- Topics
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Keywords
- chronic traumatic encephalopathy, soccer, dementia, repetitive head impacts, Alzheimer's disease, TDP-43, cerebral amyloid angiopathy, hippocampal sclerosis, corticobasal degeneration, dementia with Lewy bodies, neuropathology, concussion
- MeSH terms
- Chronic Traumatic Encephalopathy, Sequestosome-1 Protein, Aged, Aged, 80 and over, Autopsy, Brain, Calcium-Binding Proteins, Dementia, DNA-Binding Proteins, Humans, Male, Microfilament Proteins, Middle Aged, Retirement, Retrospective Studies, Soccer, Amyloid beta-Peptides, tau Proteins, alpha-Synuclein
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