Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Journal of Neurology
Published in: Journal of Neurology 7/2016

01-07-2016 | Original Communication

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

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

Published in: Journal of Neurology | Issue 7/2016

Login to get access

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.
Literature
1.
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
2.
3.
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
4.
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
5.
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
6.
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
7.
Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–455CrossRefPubMed
8.
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
9.
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.
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
Metadata
Title
The association between white-matter tract abnormalities, and neuropsychiatric and cognitive symptoms in retired professional football players with multiple concussions
Authors
Namita Multani
Ruma Goswami
Mozhgan Khodadadi
Ahmed Ebraheem
Karen D. Davis
Charles H. Tator
Richard Wennberg
David J. Mikulis
Leo Ezerins
Maria Carmela Tartaglia
Publication date
01-07-2016
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 7/2016
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-016-8141-0

Other articles of this Issue 7/2016

Journal of Neurology 7/2016 Go to the issue

Original Communication

Subclinical primary retinal pathology in neuromyelitis optica spectrum disorder

Letter to the Editors

Multiple sclerosis and chronic progressive external ophthalmoplegia associated with a large scale mitochondrial DNA single deletion

Original Communication

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

Original Communication

Variants of windmill nystagmus

Original Communication

Incidence and course of depression in multiple sclerosis in the multinational BEYOND trial

Letter to the Editors

An unusual case of acquired pedophilic behavior following compression of orbitofrontal cortex and hypothalamus by a Clivus Chordoma