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The proposed clinical features of traumatic encephalopathy syndrome have low predictive value for chronic traumatic encephalopathy pathology, raising significant concern for incorrect diagnoses of neurodegeneration in former athletes.
The discovery of chronic traumatic encephalopathy neuropathologic change in the brains of former athletes has generated an explosion in public and scientific interest. As CTE-NC can only be diagnosed postmortem, consensus diagnostic criteria have been developed for the proposed clinical correlate, that is, traumatic encephalopathy syndrome .
However, the diagnostic accuracy of TES criteria in predicting CTE-NC remains unproven and considerable concerns exist regarding the specificity of proposed clinical features. Here we reviewed antemortem clinical records for 1,038 cases in a neurodegenerative brain bank. Neuropathological evaluation for CTE-NC was then conducted in all cases. In total, 25 cases fulfilled the criteria for a diagnosis of TES, of which six demonstrated CTE-NC .
Of the remaining 1,013 cases, CTE-NC was present in seven . The diagnostic accuracy of TES for CTE-NC was driven by exposure to repetitive head impacts rather than proposed clinical features. There was no difference in the prevalence of core or supportive clinical features of TES among cases with CTE-NC compared to a matched sample.
The poor performance of TES criteria raises substantial concern for its potential negative psychological impact on current and former contact sport athletes, who may be incorrectly diagnosed with a progressive neurodegenerative pathology. Fig. 1: Chronic traumatic encephalopathy neuropathologic change and clinical features of TES.. Requests for additional de-identified individual-level data should be made to the corresponding author .
All reasonable requests will be promptly reviewed by the corresponding author and the Penn Neurodegenerative Data Sharing Committee to ensure compatibility with patient confidentiality obligations, particularly given the regional nature of the brain bank. The timeline of responses will be dictated by the ability of the Penn Neurodegenerative Data Sharing Committee to meet and adequately review data requests, but should generally be expected within 3–6 months. Provision of additional data is subject to implementation of a data use agreement.
Priemer, D. S., Iacono, D., Rhodes, C. H., Olsen, C. H. & Perl, D. P. Chronic traumatic encephalopathy in the brains of military personnel. Bieniek, K. F. et al. The second NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. Lehman, E. J., Hein, M. J., Baron, S. L. & Gersic, C. M. Neurodegenerative causes of death among retired National Football League players.
Gu, D., Ou, S. & Liu, G. Traumatic brain injury and risk of dementia and Alzheimer’s disease: a systematic review and meta-analysis. Forrest, S. L. et al. Chronic traumatic encephalopathy is absent from a european community-based aging cohort while cortical aging-related tau astrogliopathy is highly prevalent. Agrawal, S. et al.
Chronic traumatic encephalopathy and aging-related tau astrogliopathy in community-dwelling older persons with and without moderate-to-severe traumatic brain injury. Iverson, G. L., Merz, Z. C. & Terry, D. P. Examining the research criteria for traumatic encephalopathy syndrome in middle-aged men from the general population who played contact sports in high school. Lee, E. B. et al. Chronic traumatic encephalopathy is a common co-morbidity, but less frequent primary dementia in former soccer and rugby players.
Eagle, S. R. et al. Interaction of medical conditions and football exposures associated with premortem chronic traumatic encephalopathy diagnosis in former professional American football players. Iverson, G. L., Kissinger-Knox, A., Huebschmann, N. A., Castellani, R. J. & Gardner, A. J. A narrative review of psychiatric features of traumatic encephalopathy syndrome as conceptualized in the 20th century.
Iverson, G. L., Gardner, A. J., Castellani, R. J. & Kissinger-Knox, A. Applying the consensus criteria for traumatic encephalopathy syndrome retrospectively to case studies of boxers from the 20th century. Lehman, E. J., Hein, M. J. & Gersic, C. M. Suicide mortality among retired national football league players who played 5 or more seasons.
Macy, J. T., Kercher, K., Steinfeldt, J. A. & Kawata, K. Fewer US adolescents playing football and public health: a review of measures to improve safety and an analysis of gaps in the literature. Heidari, S., Babor, T. F., De Castro, P., Tort, S. & Curno, M. Sex and gender equity in research: rationale for the SAGER guidelines and recommended use.
DeLong, E. R., DeLong, D. M. & Clarke-Pearson, D. L. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. The research reported in this publication was supported by National Institutes of Health NINDS award nos. U01NS137500 , U54NS115322 , T32NS043126 and K23NS123340 ; Institute on Aging award nos. P30AG072979 , P01AG066597 and P01AG084497 ; and a Medical Research Council grant no. MR/Y008502/1 . We thank the patients and families who consented to brain donation to the University of Pennsylvania CNDR. We recognize the notable contributions of V. E. Johnson as a colleague, mentor and friend. Without her tireless dedication and passion, this work would not have been possible.
Department of Neurosurgery, Penn Center for Brain Injury and Repair, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USADepartment of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USADepartment of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA J.D. A. conceptualized and designed the study. J.D. A., J.L.
R. and R.P. D. performed the IHC experiments. J.D. A., W.S.
, A.L. C.S. , R.P. D., E.B.
L. and D.H. S. analyzed the data. A.L. C.S. provided biostatistical expertise.
J.D. A. prepared the initial draft of the paper. All authors reviewed and critically revised the paper. All authors approved the final version of the paper.
E.B. L. and D.H. S. supervised the study.thanks the anonymous reviewers for their contribution to the peer review of this work. Primary Handling Editor: Jerome Staal, in collaboration with theAll cases within the University of Pennsylvania Center for Neurodegenerative Disease Research Brain Bank collected through 2023 were considered for inclusion in the study sample.
Cases without available antemortem neurology clinical records were excluded . Of the remaining 1101 cases, those without available frontal, temporal, or parietal tissue blocks were excluded . Ultimately 1038 cases met clinical record and post-mortem tissue requirements and comprised the study sample.
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author or other rightsholder; author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
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