Incipient chronic traumatic encephalopathy in active American football players: neuropsychological assessment and brain perfusion measures.


Journal

Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175

Informations de publication

Date de publication:
Sep 2022
Historique:
received: 20 06 2021
accepted: 12 06 2022
pubmed: 25 6 2022
medline: 20 8 2022
entrez: 24 6 2022
Statut: ppublish

Résumé

Chronic traumatic encephalopathy (CTE) is a degenerative disease caused by repetitive traumatic brain injury (TBI). Because CTE can be definitely diagnosed only post-mortem, it would be important to explore clinical and radiological correlates of CTE and TBI. The aims of this study were to assess (1) the relationship between the neuropsychological profile of active American football players and the traumatic load; (2) whether traumatic brain injury associated with American football activity has a specific cerebral perfusion pattern; and (3) whether this perfusion pattern correlates with neuropsychological performances. In 20 American football players [median age [25th-75th percentile] 25.0 [21.6-31.2] years, all males], we evaluated history, traumatic load and symptoms using the TraQ (Trauma Questionnaire), and cognitive performances on neuropsychological tests. Brain perfusion was estimated using arterial spin labeling MRI and compared to a group of 19 male age-matched (28.0 [24.8-32.3] years) healthy subjects. We found different cognitive performances between American football players stratified according to field position and career length. Linemen had poorer executive, verbal, and visual performances; a career > 7 years was associated with poorer verbal fluency performances. American football players had statistically significant reduced cerebral blood flow values in sensory-motor areas in comparison with healthy controls. Poorer neuropsychological performances correlated with lower perfusion in specific brain areas. Our study seems to confirm that CTE in American football players is influenced by the field position and the career length, and correlates with lower cognitive performances linked to lower perfusion in specific brain areas.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
Chronic traumatic encephalopathy (CTE) is a degenerative disease caused by repetitive traumatic brain injury (TBI). Because CTE can be definitely diagnosed only post-mortem, it would be important to explore clinical and radiological correlates of CTE and TBI. The aims of this study were to assess (1) the relationship between the neuropsychological profile of active American football players and the traumatic load; (2) whether traumatic brain injury associated with American football activity has a specific cerebral perfusion pattern; and (3) whether this perfusion pattern correlates with neuropsychological performances.
METHODS METHODS
In 20 American football players [median age [25th-75th percentile] 25.0 [21.6-31.2] years, all males], we evaluated history, traumatic load and symptoms using the TraQ (Trauma Questionnaire), and cognitive performances on neuropsychological tests. Brain perfusion was estimated using arterial spin labeling MRI and compared to a group of 19 male age-matched (28.0 [24.8-32.3] years) healthy subjects.
RESULTS RESULTS
We found different cognitive performances between American football players stratified according to field position and career length. Linemen had poorer executive, verbal, and visual performances; a career > 7 years was associated with poorer verbal fluency performances. American football players had statistically significant reduced cerebral blood flow values in sensory-motor areas in comparison with healthy controls. Poorer neuropsychological performances correlated with lower perfusion in specific brain areas.
CONCLUSIONS CONCLUSIONS
Our study seems to confirm that CTE in American football players is influenced by the field position and the career length, and correlates with lower cognitive performances linked to lower perfusion in specific brain areas.

Identifiants

pubmed: 35750948
doi: 10.1007/s10072-022-06212-7
pii: 10.1007/s10072-022-06212-7
pmc: PMC9385804
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5383-5390

Informations de copyright

© 2022. The Author(s).

Références

Stern RA et al (2019) Tau positron-emission tomography in former National Football League players. New Engl J Med 2019. https://doi.org/10.1056/NEJMoa1900757
McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH, Lee H, Wojtowicz SM, Hall G, Baugh CM, Riley DO, Kubilus CA, Cormier KA, Jacobs MA, Martin BR, Abraham CR, Ikezu T, Reichard RR, Wolozin BL, Budson AE, Goldstein LE, Kowall NW (2013) Cantu RC (2013) The spectrum of disease in chronic traumatic encephalopathy. Brain 136(Pt 1):43–64. https://doi.org/10.1093/brain/aws307
doi: 10.1093/brain/aws307 pubmed: 23208308
Alosco ML, Stein TD, Tripodis Y, Chua AS, Kowall NW, Huber BR, Goldstein LE, Cantu RC, Katz DI, Palmisano JN, Martin B, Cherry JD, Mahar I, Killiany RJ, McClean MD, Au R, Alvarez V, Stern RA, Mez J, McKee AC (2019) Association of white matter rarefaction, arteriolosclerosis, and tau with dementia in chronic traumatic encephalopathy. JAMA Neurol. https://doi.org/10.1001/jamaneurol.2019.2244
doi: 10.1001/jamaneurol.2019.2244 pubmed: 31380975 pmcid: 6686769
Kim J, Whyte J, Patel S, Avants B, Europa E, Wang J, Slattery J, Gee JC, Coslett HB (2010) Detre JA (2009) Resting cerebral blood flow alterations in chronic traumatic brain injury: an arterial spin labeling perfusion fMRI study. J Neurotrauma 27:1399–1411. https://doi.org/10.1089/neu.2009.1215
doi: 10.1089/neu.2009.1215 pubmed: 20528163 pmcid: 2967826
Kinnunen KM, Greenwood R, Powell JH, Leech R, Hawkins PC, Bonnelle V et al (2011) (2011) White matter damage and cognitive impairment after traumatic brain injury. Brain 134(Pt 2):449–463
doi: 10.1093/brain/awq347
Liu W, Wanga B, Wolfowitza R, Yeha P, Nathana DE, Granera J, Tangd H, Pana H, Harpera J, Phame D, Oakesa TR, Frenchd LM (2013) Riedy G (2013) Perfusion deficits in patients with mild traumatic brain injury characterized by dynamic susceptibility contrast MRI. NMR Biomed 26:651–663
doi: 10.1002/nbm.2910
Grossman EJ, Jensen JH, Babb JS, Chen Q, Tabesh A, Fieremans E, Xia D, Inglese M (2013) Grossman RI (2013) Cognitive impairment in mild traumatic brain injury: a longitudinal diffusional kurtosis and perfusion imaging study. Am J Neuroradiol 34(5):951–957. https://doi.org/10.3174/ajnr.A3358
doi: 10.3174/ajnr.A3358 pubmed: 23179649 pmcid: 3908903
Querzola G, LovatiC, Mariani C, Pantoni L (2019) A semi-quantitative sport-specific assessment of recurrent traumatic brain injury: the TraQ questionnaire and its application in American Football. Neurological Sciences 2019. ISSN 1590-1874 Volume 40 Number 9. Neurol Sci (2019) 40:1909-1915 https://doi.org/10.1007/s10072-019-03853-z
Omalu B, Hamilton RL, Kamboh MI, DeKosky ST, Bailes J (2008) Chronic traumatic encephalopaty in a National Football League player: case report and emerging medicolegal practice questions
Jordan BD (2013) (2013) The clinical spectrum of sport-related traumatic brain injury - review paper, proposes clinical research diagnostic criteria for CTE. Nat Rev Neurol 9(4):222–230. https://doi.org/10.1038/nrneurol.2013.33
doi: 10.1038/nrneurol.2013.33 pubmed: 23478462
Victoroff J (2013) (2013) Traumatic encephalopathy: review and provisional research diagnostic criteria - proposed clinical research diagnostic criteria for CTE. NeuroRehabilitation 32(2):211–224. https://doi.org/10.3233/nre-130839
doi: 10.3233/nre-130839 pubmed: 23535783
Montenigro PH, Baugh CM, Daneshvar DH, Mez J, Budson AE, Au R et al (2014) Clinical subtypes of chronic traumatic encephalopathy: literature review and proposed research diagnostic criteria for traumatic encephalopathy syndrome - review: discusses historical examples of CTE, proposes research diagnostic criteria for CTE. Alzheimer’s Res Ther
Ge Y, Patel MB, Chen Q, Grossman EJ, Zhang K, Miles L, Babb JS, Reaume J & Grossman RI (2009) Assessment of thalamic perfusion in patients with mild traumatic brain injury by true FISP arterial spin labelling MR imaging at 3T. Brain Inj J. pp 666–67
Omalu BI, DeKosky ST, Minster RL, Kamboh MI, Hamilton RL (2005) Wecht CH (2005) Chronic traumatic encephalopathy in a National Football League player: part I and part II. Neurosurgery 57:128–134
doi: 10.1227/01.NEU.0000163407.92769.ED
Fagerholm ED, Hellyer PJ, Scott G, Leech R, Sharp DJ (2015) Disconnection of network hubs and cognitive impairment after traumatic brain injury. Brain 138(Pt 6):1696–709. https://doi.org/10.1093/brain/awv075
Park D (2009) Reuter-Lorenz P (2009) The adaptive brain: aging and neurocognitive scaffolding. Annu Rev Psychol 60:173–196. https://doi.org/10.1146/annurev.psych.59.103006.093656
doi: 10.1146/annurev.psych.59.103006.093656 pubmed: 19035823 pmcid: 3359129
Baugh CM, Kiernan PT, Kroshus E, Daneshvar DH, Montenigro PH, McKee AC (2015) Stern RA (2015) Frequency of head-impact–related outcomes by position in NCAA Division I collegiate football players. J Neurotrauma 32(5):314–326. https://doi.org/10.1089/neu.2014.3582
doi: 10.1089/neu.2014.3582 pubmed: 25155288 pmcid: 4628259
Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695–769
doi: 10.1111/j.1532-5415.2005.53221.x
Santangelo G, Siciliano M, Pedone R, Vitale C, Falco F, Bisogno R, Siano P, Barone P, Grossi D, Santangelo F, Trojano L (2014) Normative data for the Montreal Cognitive Assessment in an Italian population sample
Fastenau PS, Denburg NL (1999) Hufford BJ (1999) Adult norms for the Rey-Osterrieth Complex Figure Test and for supplemental recognition and matching trials from the Extended Complex Figure Test. Clin Neuropsychol 13(1):30–47. https://doi.org/10.1076/clin.13.1.30.1976
doi: 10.1076/clin.13.1.30.1976 pubmed: 10937646
Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail Making Test: normative values from 287 normal adult controls. It J Neurol Sci 17(4):305
doi: 10.1007/BF01997792
Reitan RM (1992) Trail Making Test: manual for administration and scoring. Reitan Neuropsychol Lab, Length
Carlesimo GA, Costa A, Bagoj E, Monaco M, Zabberoni S, De Rosa S, Papantonio AM, Mundi C, Caltagirone C (2013) Standardization and normative data obtained in the Italian population for a new verbal fluency instrument, the phonemic/semantic alternate fluency test. Neurol Sci 35(3). https://doi.org/10.1007/s10072-013-1520-8
Novelli G, Papagno C, Capitani E, Laiacona M, Vallar G, Cappa SF (1986) Tre test clinici di ricerca e produzione lessicale. Taratura su 320 soggetti normali. Arch Psicol Neurol Psichiatr 47(4):477–506
Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A (2002) A short version of the Stroop test: normative data in an Italian population sample. Nuova Riv Neurol
Nocentini U, Giordano A, Di Vincenzo S, Panella M, Pasqualetti P(2006) The symbol digit modalities test - oral version: Italian normative data. Funct Neurol 21(2):93–6
Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A (2002) De Stefano N (2002) Accurate, robust and automated longitudinal and crosssectional brain change analysis. Neuroimage 17(1):479–489
doi: 10.1006/nimg.2002.1040
Chappell MA, Groves AR, Whitcher B et al (2009) (2009) Variational Bayesian inference for a nonlinear forward model. IEEE Trans Signal Proc 57:223–236
doi: 10.1109/TSP.2008.2005752
Wang DJ, Alger JR, Qiao JX, Gunther M, Pope WB, Saver JL, Salamon N (2013) Liebeskind DS (2013) Multi-delay multi-parametric arterial spin-labeled perfusion MRI in acute ischemic stroke - comparison with dynamic susceptibility contrast enhanced perfusion imaging. UCLA Stroke Investigators - Neuroimage Clin 3:1–7
doi: 10.1016/j.nicl.2013.06.017
Winkler AM, Ridgway GR, Webster MA, Smith SM (2014) Nichols TE (2014) Permutation inference for the general linear model. Neuroimage 15(92):381–397. https://doi.org/10.1016/j.neuroimage.2014.01.060
doi: 10.1016/j.neuroimage.2014.01.060
Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29(4):1165–1188
doi: 10.1214/aos/1013699998
Collins MW, Grindel SH, Lovell MR et al (1999) (1999) Relationship between concussion and neuropsychological performance in college football players. JAMA 282:964–970
doi: 10.1001/jama.282.10.964
Kutner KC, Ehrlanger D, Tsai J et al (2000) (2000) Lower cognitive performance of older football players possessing apolipoprotein E e4. Neurosurg 47:651–658
Rabadi MH (2001) Jordan BD (2001) The cumulative effect of repetitive concussion in sports. Clin J Sport Med 11(3):194–198. https://doi.org/10.1097/00042752-200107000-00011
doi: 10.1097/00042752-200107000-00011 pubmed: 11495325
Omalu BI, DeKosky ST, Hamilton RL, Minster RL, Kamboh MI, Shakir AM, Wecht CH (2006) Chronic traumatic encephalopathy in a national football league player: part II. Neurosurgery. 2006 59(5):1086–92; discussion 1092–3. https://doi.org/10.1227/01.NEU.0000245601.69451.27
Macciocchi S, Barth J, Littlefield L, Cantu R (2001) Multiple concussions and neuropsychological functioning in collegiate football players. J Athl Train 36(3): 303–306
Hendrich KS, Kochanek P. M., Williams D. S., Schiding J. K., Marion D. W., Ho C. (1999). Early perfusion after controlled cortical impact in rats: quantification by arterial spin-labeled MRI and the influence of spin-lattice relaxation time heterogeneity. Magn Reson Med. pp 673–681. https://doi.org/10.1002/(SICI)1522-2594(199910)42:4<673::AID-MRM8>3.0.CO;2-B
Cheng JL, Yang YJ, Li HL, Wang J, Wang MH, Zhang Y (2010) In vivo tracing of superparamagnetic iron oxide-labeled bone marrow mesenchymal stem cells transplanted for traumatic brain injury by susceptibility weighted imaging in a rat model. Chin J Traumatol 13:173–177
pubmed: 20515596
Zhang J, Zhang Y, Wang J, Cai P, Luo C, Qian Z et al (2010) Characterizing iron deposition in Parkinson’s disease using susceptibility-weighted imaging: an in vivo MR study. Brain Res 1330:124–130
doi: 10.1016/j.brainres.2010.03.036
Turner RC, Lucke-Wold BP, Robson MJ, Omalu BI, Petraglia AL, Bailes JE (2013) Repetitive traumatic brain injury and development of chronic traumatic encephalopathy: a potential role for biomarkers in diagnosis, prognosis, and treatment? Front Neurol. 3: Article 186

Auteurs

Giacomo Querzola (G)

'Luigi Sacco' Department of Biomedical and Clinical Sciences, University of Milan, Via Giovanni Battista Grassi, 74, 20157, Milan, Italy. giacomo.querzola@unimi.it.

Carlo Lovati (C)

Headache Center, Neurology Unit, Luigi Sacco Hospital, Milan, Italy.

Maria M Laganà (MM)

IRCCS, Fondazione Don Carlo Gnocchi ONLUS, Milan, Italy.

Alice Pirastru (A)

IRCCS, Fondazione Don Carlo Gnocchi ONLUS, Milan, Italy.

Francesca Baglio (F)

IRCCS, Fondazione Don Carlo Gnocchi ONLUS, Milan, Italy.

Leonardo Pantoni (L)

'Luigi Sacco' Department of Biomedical and Clinical Sciences, University of Milan, Via Giovanni Battista Grassi, 74, 20157, Milan, Italy.

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