nach oben

Erschienen in:

03.05.2016 | Original Communication

The association between white-matter tract abnormalities, and neuropsychiatric and cognitive symptoms in retired professional football players with multiple concussions

verfasst von: Namita Multani, Ruma Goswami, Mozhgan Khodadadi, Ahmed Ebraheem, Karen D. Davis, Charles H. Tator, Richard Wennberg, David J. Mikulis, Leo Ezerins, Maria Carmela Tartaglia

Erschienen in: Journal of Neurology | Ausgabe 7/2016

Einloggen, um Zugang zu erhalten

Abstract

Retired professional athletes, who have suffered repetitive concussions, report symptoms of depression, anxiety, and memory impairment over time. Moreover, recent imaging data suggest chronic white-matter tract deterioration in sport-related concussion. The aim of this study is to evaluate the impact of repetitive concussions in retired professional football players on white-matter tracts, and relate these changes to neuropsychological function. All subjects (18 retired professional football players and 17 healthy controls) underwent imaging, neuropsychological assessment, and reported on concussion-related symptoms. Whole brain tract-based spatial statistics analysis revealed increased axial diffusivity in the right hemisphere of retired players in the (1) superior longitudinal fasciculus (SLF), (2) corticospinal tract, and (3) anterior thalamic radiations, suggesting chronic axonal degeneration in these tracts. Moreover, retired players report significantly higher neuropsychiatric and cognitive symptoms than healthy controls, and worsening of these symptoms since their last concussion. Loss of integrity in the right SLF significantly correlated with participants’ visual learning ability. In sum, these results suggest that repetitive concussions in retired professional football players are associated with focal white-matter tract abnormalities that could explain some of the neuropsychiatric symptoms and cognitive deficits experienced by these retired athletes.

Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci: MN 34:51–61CrossRefPubMed

Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267CrossRefPubMedPubMedCentral

Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson, Ser B 111:209–219CrossRef

Baugh CM, Stamm JM, Riley DO, Gavett BE, Shenton ME, Lin A, Nowinski CJ, Cantu RC, McKee AC, Stern RA (2012) Chronic traumatic encephalopathy: neurodegeneration following repetitive concussive and subconcussive brain trauma. Brain Imaging Behav 6:244–254CrossRefPubMed

Bazarian JJ, Zhu T, Blyth B, Borrino A, Zhong J (2012) Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magn Reson Imaging 30:171–180CrossRefPubMed

Bazarian JJ, Zhu T, Zhong J, Janigro D, Rozen E, Roberts A, Javien H, Merchant-Borna K, Abar B, Blackman EG (2014) Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts. PLoS One 9:e94734CrossRefPubMedPubMedCentral

Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–455CrossRefPubMed

Belanger HG, Spiegel E, Vanderploeg RD (2010) Neuropsychological performance following a history of multiple self-reported concussions: a meta-analysis. J Int Neuropsychol Soc: JINS 16:262–267CrossRefPubMed

Bendlin BB, Carlsson CM, Johnson SC, Zetterberg H, Blennow K, Willette AA, Okonkwo OC, Sodhi A, Ries ML, Birdsill AC, Alexander AL, Rowley HA, Puglielli L, Asthana S, Sager MA (2012) CSF T-Tau/Abeta42 predicts white matter microstructure in healthy adults at risk for Alzheimer’s disease. PLoS One 7:e37720CrossRefPubMedPubMedCentral

10.

Biasca N, Maxwell WL (2007) Minor traumatic brain injury in sports: a review in order to prevent neurological sequelae. Prog Brain Res 161:263–291CrossRefPubMed

11.

Bieniek KF, Ross OA, Cormier KA, Walton RL, Soto-Ortolaza A, Johnston AE, DeSaro P, Boylan KB, Graff-Radford NR, Wszolek ZK, Rademakers R, Boeve BF, McKee AC, Dickson DW (2015) Chronic traumatic encephalopathy pathology in a neurodegenerative disorders brain bank. Acta Neuropathol 130:877–889CrossRefPubMed

12.

Chappell MH, Ulug AM, Zhang L, Heitger MH, Jordan BD, Zimmerman RD, Watts R (2006) Distribution of microstructural damage in the brains of professional boxers: a diffusion MRI study. J Magn Reson Imaging: JMRI 24:537–542CrossRefPubMed

13.

Chechlacz M, Gillebert CR, Vangkilde SA, Petersen A, Humphreys GW (2015) Structural variability within frontoparietal networks and individual differences in attentional functions: an approach using the theory of visual attention. J Neurosci 35:10647–10658CrossRefPubMedPubMedCentral

14.

Ciccarelli O, Catani M, Johansen-Berg H, Clark C, Thompson A (2008) Diffusion-based tractography in neurological disorders: concepts, applications, and future developments. Lancet Neurol 7:715–727CrossRefPubMed

15.

Cubon VA, Putukian M, Boyer C, Dettwiler A (2011) A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. J Neurotrauma 28:189–201CrossRefPubMedPubMedCentral

16.

De Schotten MT, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DG, Catani M (2011) A lateralized brain network for visuospatial attention. Nat Neurosci 14:1245–1246CrossRef

17.

Donovan V, Kim C, Anugerah AK, Coats JS, Oyoyo U, Pardo AC, Obenaus A (2014) Repeated mild traumatic brain injury results in long-term white-matter disruption. J Cereb Blood Flow Metab: Off J Int Soc Cereb Blood Flow Metab 34:715–723CrossRef

18.

Ellemberg D, Henry LC, Macciocchi SN, Guskiewicz KM, Broglio SP (2009) Advances in sport concussion assessment: from behavioral to brain imaging measures. J Neurotrauma 26:2365–2382CrossRefPubMed

19.

Geary EK, Kraus MF, Pliskin NH, Little DM (2010) Verbal learning differences in chronic mild traumatic brain injury. J Int Neuropsychol Soc: JINS 16:506–516CrossRefPubMed

20.

Gennarelli TA, Thibault LE, Graham DI (1998) Diffuse axonal injury: an important form of traumatic brain damage. Neuroscientist 4:202–215CrossRef

21.

Goswami R, Dufort P, Tartaglia MC, Green RE, Crawley A, Tator CH, Wennberg R, Mikulis DJ, Keightley M, Davis KD (2015) Frontotemporal correlates of impulsivity and machine learning in retired professional athletes with a history of multiple concussions. Brain Struct Funct 1–15. doi:10.1007/s00429-015-1012-0

22.

Graham DI, McIntosh TK, Maxwell WL, Nicoll JA (2000) Recent advances in neurotrauma. J Neuropathol Exp Neurol 59:641–651CrossRefPubMed

23.

Guskiewicz KM, McCrea M, Marshall SW, Cantu RC, Randolph C, Barr W, Onate JA, Kelly JP (2003) Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA, J Am Med Assoc 290:2549–2555CrossRef

24.

Hazrati LN, Tartaglia MC, Diamandis P, Davis KD, Green RE, Wennberg R, Wong JC, Ezerins L, Tator CH (2013) Absence of chronic traumatic encephalopathy in retired football players with multiple concussions and neurological symptomatology. Front Hum Neurosci 7:222CrossRefPubMedPubMedCentral

25.

Hoeft F, Barnea-Goraly N, Haas BW, Golarai G, Ng D, Mills D, Korenberg J, Bellugi U, Galaburda A, Reiss AL (2007) More is not always better: increased fractional anisotropy of superior longitudinal fasciculus associated with poor visuospatial abilities in Williams syndrome. J Neurosci 27:11960–11965CrossRefPubMed

26.

Holdnack HA (2001) Wechsler Test of Adult Reading: WTAR. The Psychological Corporation, San Antonio

27.

Hua K, Zhang J, Wakana S, Jiang H, Li X, Reich DS, Calabresi PA, Pekar JJ, van Zijl PC, Mori S (2008) Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. Neuroimage 39:336–347CrossRefPubMed

28.

Iverson GL, Gardner AJ, McCrory P, Zafonte R, Castellani RJ (2015) A critical review of chronic traumatic encephalopathy. Neurosci Biobehav Rev 56:276–293CrossRefPubMed

29.

Jessen F, Wolfsgruber S, Wiese B, Bickel H, Mosch E, Kaduszkiewicz H, Pentzek M, Riedel-Heller SG, Luck T, Fuchs A, Weyerer S, Werle J, van den Bussche H, Scherer M, Maier W, Wagner M, German Study on Aging C, Dementia in Primary Care P (2014) AD dementia risk in late MCI, in early MCI, and in subjective memory impairment. Alzheimer’s Dement J Alzheimer’s Assoc 10:76–83CrossRef

30.

Johnson VE, Stewart W, Smith DH (2013) Axonal pathology in traumatic brain injury. Exp Neurol 246:35–43CrossRefPubMed

31.

Johnston KM, Ptito A, Chankowsky J, Chen JK (2001) New frontiers in diagnostic imaging in concussive head injury. Clin J Sport Med: Off J Can Acad Sport Med 11:166–175CrossRef

32.

Koerte IK, Ertl-Wagner B, Reiser M, Zafonte R, Shenton ME (2012) White matter integrity in the brains of professional soccer players without a symptomatic concussion. JAMA, J Am Med Assoc 308:1859–1861CrossRef

33.

Koerte IK, Kaufmann D, Hartl E, Bouix S, Pasternak O, Kubicki M, Rauscher A, Li DK, Dadachanji SB, Taunton JA, Forwell LA, Johnson AM, Echlin PS, Shenton ME (2012) 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 33(E3):1–7PubMed

34.

Kraus MF, Susmaras T, Caughlin BP, Walker CJ, Sweeney JA, Little DM (2007) White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain: J Neurol 130:2508–2519CrossRef

35.

Kryscio RJ, Abner EL, Cooper GE, Fardo DW, Jicha GA, Nelson PT, Smith CD, Van Eldik LJ, Wan L, Schmitt FA (2014) Self-reported memory complaints: implications from a longitudinal cohort with autopsies. Neurology 83:1359–1365CrossRefPubMedPubMedCentral

36.

Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS Jr, Pandya DN (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex 15:854–869CrossRefPubMed

37.

Mamah D, Conturo TE, Harms MP, Akbudak E, Wang L, McMichael AR, Gado MH, Barch DM, Csernansky JG (2010) Anterior thalamic radiation integrity in schizophrenia: a diffusion-tensor imaging study. Psychiatry Res 183:144–150CrossRefPubMed

38.

McAllister TW, Ford JC, Flashman LA, Maerlender A, Greenwald RM, Beckwith JG, Bolander RP, Tosteson TD, Turco JH, Raman R, Jain S (2014) Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology 82:63–69CrossRefPubMedPubMedCentral

39.

McKee AC, Cantu RC, Nowinski CJ, Hedley-Whyte ET, Gavett BE, Budson AE, Santini VE, Lee HS, Kubilus CA, Stern RA (2009) Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 68:709–735CrossRefPubMedPubMedCentral

40.

McKee AC, Daneshvar DH, Alvarez VE, Stein TD (2014) The neuropathology of sport. Acta Neuropathol 127:29–51CrossRefPubMed

41.

Mendez MF (1995) The neuropsychiatric aspects of boxing. Int J Psychiatry Med 25:249–262CrossRefPubMed

42.

Mitchell AJ, Beaumont H, Ferguson D, Yadegarfar M, Stubbs B (2014) Risk of dementia and mild cognitive impairment in older people with subjective memory complaints: meta-analysis. Acta Psychiatr Scand 130:439–451CrossRefPubMed

43.

Mori S, Wakana S, van Zijl PC, Nagae-Poetscher LM (2005) MRI Atlas of Human White Matte. Elsevier, Amsterdam

44.

Naunheim RS, Standeven J, Richter C, Lewis LM (2000) Comparison of impact data in hockey, football, and soccer. J Trauma 48:938–941CrossRefPubMed

45.

Niogi SN, Mukherjee P, Ghajar J, Johnson C, Kolster RA, Sarkar R, Lee H, Meeker M, Zimmerman RD, Manley GT, McCandliss BD (2008) Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. AJNR Am J Neuroradiol 29:967–973CrossRefPubMed

46.

Omalu BI, Bailes J, Hammers JL, Fitzsimmons RP (2010) Chronic traumatic encephalopathy, suicides and parasuicides in professional American athletes: the role of the forensic pathologist. Am J Forensic Med Pathol 31:130–132CrossRefPubMed

47.

Perez AM, Adler J, Kulkarni N, Strain JF, Womack KB, Diaz-Arrastia R, Marquez de la Plata CD (2014) Longitudinal white matter changes after traumatic axonal injury. J Neurotrauma 31:1478–1485CrossRefPubMedPubMedCentral

48.

Pontifex MB, O’Connor PM, Broglio SP, Hillman CH (2009) The association between mild traumatic brain injury history and cognitive control. Neuropsychologia 47:3210–3216CrossRefPubMed

49.

Reisberg B, Shulman MB, Torossian C, Leng L, Zhu W (2010) Outcome over seven years of healthy adults with and without subjective cognitive impairment. Alzheimer’s Dement J Alzheimer’s Assoc 6:11–24CrossRef

50.

Rey A (1941) Psychological examination of traumatic encephalopathy. Archives de Psychologie 28:215–285

51.

Song S-K, Sun S-W, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water. NeuroImage 17:1429–1436CrossRefPubMed

52.

Stern RA, Riley DO, Daneshvar DH, Nowinski CJ, Cantu RC, McKee AC (2011) Long-term consequences of repetitive brain trauma: chronic traumatic encephalopathy. PM & R: J Inj Funct Rehabil 3:S460–467CrossRef

53.

Tremblay S, Henry LC, Bedetti C, Larson-Dupuis C, Gagnon JF, Evans AC, Theoret H, Lassonde M, Beaumont LD (2014) Diffuse white matter tract abnormalities in clinically normal ageing retired athletes with a history of sports-related concussions. Brain: J Neurol 137:2997–3011CrossRef

54.

van der Flier WM, van Buchem MA, Weverling-Rijnsburger AW, Mutsaers ER, Bollen EL, Admiraal-Behloul F, Westendorp RG, Middelkoop HA (2004) Memory complaints in patients with normal cognition are associated with smaller hippocampal volumes. J Neurol 251:671–675CrossRefPubMed

55.

Wilson BA (2000) Compensating for cognitive deficits following brain injury. Neuropsychol Rev 10:233–243CrossRefPubMed

56.

Yamada K, Sakai K, Akazawa K, Yuen S, Nishimura T (2009) MR tractography: a review of its clinical applications. Magn Reson Med Sci: MRMS: Off J Japan Soc Magn Reson Med 8:165–174

57.

Zhang L, Heier LA, Zimmerman RD, Jordan B, Ulug AM (2006) Diffusion anisotropy changes in the brains of professional boxers. AJNR Am J Neuroradiol 27:2000–2004PubMed

Titel: The association between white-matter tract abnormalities, and neuropsychiatric and cognitive symptoms in retired professional football players with multiple concussions
verfasst von: Namita Multani
Ruma Goswami
Mozhgan Khodadadi
Ahmed Ebraheem
Karen D. Davis
Charles H. Tator
Richard Wennberg
David J. Mikulis
Leo Ezerins
Maria Carmela Tartaglia
Publikationsdatum: 03.05.2016
Verlag: Springer Berlin Heidelberg
Erschienen in: Journal of Neurology / Ausgabe 7/2016
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-016-8141-0

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Demenzkranke durch Antipsychotika vielfach gefährdet

23.04.2024 Demenz Nachrichten

Wenn Demenzkranke aufgrund von Symptomen wie Agitation oder Aggressivität mit Antipsychotika behandelt werden, sind damit offenbar noch mehr Risiken verbunden als bislang angenommen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 7/2016

Validation of a clinical practice-based algorithm for the diagnosis of autosomal recessive cerebellar ataxias based on NGS identified cases

The interrelationship between disease severity, dynamic stability, and falls in cerebellar ataxia

Subclinical primary retinal pathology in neuromyelitis optica spectrum disorder

EGR2 mutation enhances phenotype spectrum of Dejerine–Sottas syndrome

A novel MYH2 mutation in family members presenting with congenital myopathy, ophthalmoplegia and facial weakness