Top

Neurological Sciences

Published in:

Open Access 24-06-2022 | Central Nervous System Trauma | Original Article

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

Authors: Giacomo Querzola, Carlo Lovati, Maria M. Laganà, Alice Pirastru, Francesca Baglio, Leonardo Pantoni

Published in: Neurological Sciences | Issue 9/2022

Abstract

Background and aims

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

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

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

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.

Available only for authorised users

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/aws307CrossRefPubMed

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.2019.2244CrossRefPubMedPubMedCentral

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.2009.1215CrossRefPubMedPubMedCentral

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):449–463CrossRef

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 26:651–663CrossRef

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.A3358CrossRefPubMedPubMedCentral

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) 40:1909-1915https://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

10.

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.2013.33CrossRefPubMed

11.

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-130839CrossRefPubMed

12.

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

13.

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

14.

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 57:128–134CrossRef

15.

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

16.

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.59.103006.093656CrossRefPubMedPubMedCentral

17.

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.2014.3582CrossRefPubMedPubMedCentral

18.

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):695–769CrossRef

19.

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

20.

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.13.1.30.1976CrossRefPubMed

21.

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):305CrossRef

22.

Reitan RM (1992) Trail Making Test: manual for administration and scoring. Reitan Neuropsychol Lab, Length

23.

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

24.

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

25.

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

26.

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

27.

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):479–489CrossRef

28.

Chappell MA, Groves AR, Whitcher B et al (2009) (2009) Variational Bayesian inference for a nonlinear forward model. IEEE Trans Signal Proc 57:223–236CrossRef

29.

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 3:1–7CrossRef

30.

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.2014.01.060CrossRef

31.

Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29(4):1165–1188CrossRef

32.

Collins MW, Grindel SH, Lovell MR et al (1999) (1999) Relationship between concussion and neuropsychological performance in college football players. JAMA 282:964–970CrossRef

33.

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

34.

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/10.1097/00042752-200107000-00011CrossRefPubMed

35.

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

36.

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

37.

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

38.

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 13:173–177PubMed

39.

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 1330:124–130CrossRef

40.

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

Title: Incipient chronic traumatic encephalopathy in active American football players: neuropsychological assessment and brain perfusion measures
Authors: Giacomo Querzola
Carlo Lovati
Maria M. Laganà
Alice Pirastru
Francesca Baglio
Leonardo Pantoni
Publication date: 24-06-2022
Publisher: Springer International Publishing
Keywords: Central Nervous System Trauma
Encephalopathy
Published in: Neurological Sciences / Issue 9/2022
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-022-06212-7

At a glance: The STEP trials

Springer Medicine

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

Abstract

Background and aims

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Background and aims

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 9/2022

The Italian tremor Network (TITAN): rationale, design and preliminary findings

Episodic memory in progressive supranuclear palsy: a neuropsychological and neuroimaging study

Anti-seizure medication treatment and outcomes in acute ischemic stroke patients undergoing continuous EEG monitoring

The impact of headache symptoms in a population of Italian university students during the COVID period: an observational study based on 4926 cases

Cognitive function in untreated subjects with mild hyperphenylalaninemia: a systematic review

The use of corticosteroids in patients with COVID-19 vaccine–related cerebral venous thrombosis