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Soccer Heading Is Associated with White Matter Microstructural and Cognitive Abnormalities
Open accessAbstract
PURPOSE: To investigate the association of soccer heading with subclinical evidence of traumatic brain injury. MATERIALS AND METHODS: With institutional review board approval and compliance with HIPAA guidelines, 37 amateur soccer players (mean age, 30.9 years; 78% [29] men, 22% [eight] women) gave written informed consent and completed a questionnaire to quantify heading in the prior 12 months and lifetime concussions. Diffusion-tensor magnetic resonance (MR) imaging at 3.0 T was performed (32 directions; b value, 800 sec/mm(2); 2 × 2 × 2-mm voxels). Cognitive function was measured by using a computerized battery of tests. Voxelwise linear regression (heading vs fractional anisotropy [FA]) was applied to identify significant regional associations. FA at each location and cognition were tested for a nonlinear relationship to heading by using an inverse logit model that incorporated demographic covariates and history of concussion. RESULTS: Participants had headed 32-5400 times (median, 432 times) over the previous year. Heading was associated with lower FA at three locations in temporo-occipital white matter with a threshold that varied according to location (885-1550 headings per year) (P < .00001). Lower levels of FA were also associated with poorer memory scores (P < .00001), with a threshold of 1800 headings per year. Lifetime concussion history and demographic features were not significantly associated with either FA or cognitive performance. CONCLUSION: Heading is associated with abnormal white matter microstructure and with poorer neurocognitive performance. This relationship is not explained by a history of concussion.
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“Recently, soccer players who head the ball more than 1,800 times per year were found to have microstructural abnormalities in the temporo-occipital white matter on DTI that correlated with poorer memory scores [111].”
From The neuropathology of sport (2014) · cites this paper as [111]
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“The assumption is that the lighter synthetic ball may also put modern footballers at risk of subconcussion and CTE is supported by the radiological findings of abnormal white matter microstructure in young footballers who headed the ball frequently [26] and the post-mortem finding of CTE in a 29-year-old footballer wi…”
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Ling, H., Hardy, J., & Zetterberg, H. (2015) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2015.03.012 · Cited by 197
“Soccer players who head the ball more than 1800 times per year were found to have microstructural abnormalities in the temporo-occipital white matter on diffusion tensor imaging correlating with poorer memory scores (Lipton et al., 2013).”
Subconcussive head impacts in sport: A systematic review of the evidence
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Evidence for Acute Electrophysiological and Cognitive Changes Following Routine Soccer Heading
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“As well as increased corticomotor inhibition, parameters of memory function were altered following the heading protocol, consistent with a recent report of a relationship betweenmemory function and history of heading in soccer (Lipton et al., 2013).”
BackgroundAsken, B. M., DeKosky, S. T., Clugston, J. R., Jaffee, M. S., & Bauer, R. M. (2017) · Brain Imaging and Behavior · doi:10.1007/s11682-017-9708-9 · Cited by 167
Neuroimaging Biomarkers in Mild Traumatic Brain Injury (mTBI)
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“Nonetheless, abnormal WM findings have been reported in physician-observed concussion from hockeyrelated injury as well as soccer players without symptomatic concussion, but with history of head and soccer ball impact (Koerte et al. 2012b, a; Lipton et al. 2013).”
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BackgroundAltered Neurochemistry in Former Professional Soccer Players without a History of Concussion
Koerte, I. K., Lin, A. P., Muehlmann, M., Merugumala, S. K., Liao, H. V., Starr, T. C., Kaufmann, D., Mayinger, M. C., Steffinger, D., Fisch, B., et al. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2014.3715 · Cited by 173
An Evidence-Based Discussion of Heading the Ball and Concussions in High School Soccer
Comstock, R. D., Currie, D. W., Pierpoint, L. A., Grubenhoff, J. A., & Fields, S. K. (2015) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2015.1062 · Cited by 157
A review of neuroimaging findings in repetitive brain trauma
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“A study by Lipton et al (88) also used DTI to study white matter alterations in amateur players and found a nonlinear association between the number of headings performed during the previous 12 months and lower FA in temporo-occipital white matter, suggesting a threshold dose–response relationship.”
BackgroundCortical thinning in former professional soccer players
Koerte, I. K., Mayinger, M. C., Muehlmann, M., Kaufmann, D., Lin, A. P., Steffinger, D., Fisch, B., Rauchmann, B., Immler, S., Karch, S., et al. (2015) · Brain Imaging and Behavior · doi:10.1007/s11682-015-9442-0 · Cited by 148
“Frequently heading a soccer ball has been discussed as a source of subconcussive head impact in soccer (Koerte et al. 2012, 2015b; Lipton and Kim 2013; Jordan et al. 1996).”
BackgroundWhite Matter Compromise in Veterans Exposed to Primary Blast Forces
Taber, K. H., Hurley, R. A., Haswell, C. C., Rowland, J. A., Hurt, S. D., Lamar, C. D., & Morey, R. A. (2014) · Journal of Head Trauma Rehabilitation · doi:10.1097/htr.0000000000000030 · Cited by 129
Chronic Traumatic Encephalopathy: Historical Origins and Current Perspective
Montenigro, P. H., Stein, T. D., Cantu, R. C., & Stern, R. A. (2015) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-032814-112814 · Cited by 133
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“(17) has found that soccer heading is associated with poorer neurocognitive performance and abnormal white matter microstructure; a relationship not explained by concussion history or demographics.”
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“31 In college athletesexhibiting prolonged symptomsafter SRC, increased MD has been reported in parts of the left inferior/superior longitudinal and fronto-occipital fasciculi, the retrolenticular part of the internal capsule, and posterior thalamic and acoustic radiations.”
Rosenkrantz, A. B., Ayoola, A., Singh, K., & Duszak, R. (2017) · Academic Radiology · doi:10.1016/j.acra.2016.11.019 · Cited by 117
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“O n average, a female collegiate soccer player experiences 2 to 7 head impacts during a game and 2 to 4 head impacts during a practice, thereby accumulating hundreds of impacts over a season and thousands over a career.(4) Soccer heading is usually unremarkable in that it does not present with the typical signs and sy…”
BackgroundTraumatic brain injury and cognition
Cristofori, I., & Levin, H. S. (2015) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63521-1.00037-6 · Cited by 115
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“…are significantly different resting neural networks identifiable on fMRI (Breedlove et al. 2012) even after clinical concussion resolves (Johnson et al. 2011; Talavage et al. 2013), or DTI abnormalities as has been identified in soccer players (Lipton et al. 2013), consistent with lasting injury.”
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“Keywords: American football; Chronic traumatic encephalopathy; Repetitive head impacts; Tau; Total tau; Plasma; Head trauma”
BackgroundUse of Brain Biomechanical Models for Monitoring Impact Exposure in Contact Sports
Ji, S., Ghajari, M., Mao, H., Kraft, R. H., Hajiaghamemar, M., Panzer, M. B., Willinger, R., Gilchrist, M. D., Kleiven, S., & Stitzel, J. D. (2022) · Annals of Biomedical Engineering · doi:10.1007/s10439-022-02999-w · Cited by 98
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“Recent evidence suggests, however, that RHI, especially if they occur in close proximity in time, may lead to structural and functional brain alterations and clinical impairment even if there are no acute symptoms 2–5 (for review, see Koerte and associates 6 ).”
Systematic review and meta-analysis of the effects of football heading
Kontos, A. P., Braithwaite, R. E., Chrisman, S. P. D., McAllister-Deitrick, J., Symington, L., Reeves, V. L., & Collins, M. W. (2016) · British Journal of Sports Medicine · doi:10.1136/bjsports-2016-096276 · Cited by 91
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“This pattern is consistent with the notion that the heading-neuropsychological function relationship entails a threshold effect, as suggested by our earlier findings (Lipton et al., 2013).”
BackgroundResultInfluentialSelf-citationSex Differences in Anthropometrics and Heading Kinematics Among Division I Soccer Athletes
Bretzin, A. C., Mansell, J. L., Tierney, R., & McDevitt, J. K. (2016) · Sports Health A Multidisciplinary Approach · doi:10.1177/1941738116678615 · Cited by 85
“Heading is inherent in soccer, with amateur soccer athletes self-reporting between 276 and 1096 headers per year.(17) 678615 SPHXXX10.”
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Sollmann, N., Echlin, P. S., Schultz, V., Viher, P. V., Lyall, A. E., Tripodis, Y., Kaufmann, D., Härtl, E., Kinzel, P., Forwell, L. A., et al. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.11.020 · Cited by 81
“Evidence suggests that RSHI may also lead to detectable WM alterations (Koerte et al., 2012a, 2012b; Lipton et al., 2013; McAllister et al., 2014).”
BackgroundConcussion—Mild Traumatic Brain Injury
Kamins, J., & Giza, C. C. (2016) · Neurosurgery Clinics of North America · doi:10.1016/j.nec.2016.05.005 · Cited by 81
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Biomechanical Perspectives on Concussion in Sport
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Advanced biomarkers of pediatric mild traumatic brain injury: Progress and perils
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“, 2014) and heading the ball in soccer players (Lipton et al., 2013).”
Rubin, T. G., Catenaccio, E., Fleysher, R., Hunter, L. E., Lubin, N., Stewart, W. F., Kim, M., Lipton, R. B., & Lipton, M. L. (2018) · Radiology · doi:10.1148/radiol.2018180217 · Cited by 75
“The frequency of heading during the previous 12 months was estimated with use of a previously validated structured questionnaire (3,4).”
BackgroundMethodResultSelf-citationHead Impact Exposure During a Weekend Youth Soccer Tournament
Chrisman, S. P. D., Donald, C. L. M., Friedman, S. D., Andre, J. B., Rowhani‐Rahbar, A., Drescher, S., Stein, E. M., Holm, M., Evans, N., Poliakov, A. V., et al. (2016) · Journal of Child Neurology · doi:10.1177/0883073816634857 · Cited by 74
“Past medical history (n, %) LD and ADHD 1 (6) Migraine 1 (6) Anxiety 1 (6) Family income (n, %) 70-100k 2 (12) 100k 15 (88) Parental marital status (n, %) Separated or divorced 1 (6) Married 16 (94) Parental education (n, %) Some college, no degree 3 (17.”
BackgroundMinimizing Head Acceleration in Soccer: A Review of the Literature
Caccese, J. B., & Kaminski, T. W. (2016) · Sports Medicine · doi:10.1007/s40279-016-0544-7 · Cited by 74
Head Impact Biomechanics in Women’s College Soccer
Lynall, R. C., Clark, M., Grand, E., Stucker, J. C., Littleton, A. C., Aguilar, A. J., Petschauer, M. A., Teel, E. F., & Mihalik, J. P. (2016) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000951 · Cited by 74
“(18) has attempted to understand this phenomenon and has broadly suggested that heading is associated with abnormal white matter microstructure.”
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“…Hutchison, Cusimano, Comper, & Schweizer, 2014), but some studies have reported depressed neuropsychological performance (Caccese & Kaminski, 2016a; Lipton et al., 2013; Maher et al., 2014), increased biochemical markers of brain damage (Dorminy et al., 2015; Koerte et al., 2015; Maher et al.,…”
BackgroundHeading in soccer increases serum neurofilament light protein and SCAT3 symptom metrics
Wallace, C., Smirl, J. D., Zetterberg, H., Blennow, K., Bryk, K. N., Burma, J. S., Dierijck, J. K., Wright, A. D., & van Donkelaar, P. (2018) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2018-000433 · Cited by 71
“…diffusion tensor MRI, thought to reflect white matter structural disruption, has been shown to relate to the number of headers performed in a year; 8 however, when expanded over the length of a career no differences on MRI were seen between soccer players and control (ie, track and field)…”
BackgroundAssociation of Sex With Adolescent Soccer Concussion Incidence and Characteristics
Bretzin, A. C., Covassin, T., Wiebe, D. J., & Stewart, W. B., Jr. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.8191 · Cited by 71
Potential for use of creatine supplementation following mild traumatic brain injury
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Symptoms from repeated intentional and unintentional head impact in soccer players
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Self-citationWirsching, A., Chen, Z., Bevilacqua, Z. W., Huibregtse, M. E., & Kawata, K. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2018.5836 · Cited by 69
“…sports can sustain several hundred up to over one thousand subconcussive head impacts annually from soccer heading and American football tackling, 1–3 which have been shown to trigger degenerative responses in the brain, characterized by axonal growth cone collapse, tau protein disruption,…”
Effects of Soccer Heading on Brain Structure and Function
Rodrigues, A. C., Lasmar, R. C. P., & Caramelli, P. (2016) · Frontiers in Neurology · doi:10.3389/fneur.2016.00038 · Cited by 69
“(15) investigated white matter microstructure in male and female amateur soccer players, with a mean age of 30.”
BackgroundInfluentialBeaudouin, F., Gioftsidou, A. F., Larsen, M. N., LEMMINK, K. A. P. M., Drust, B., Modena, R., Espinola, J. R., Meiu, M., Vouillamoz, M., & Meyer, T. (2020) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.13694 · Cited by 68
Ntikas, M., Binkofski, F., Shah, N. J., & Ietswaart, M. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19127098 · Cited by 67
“However, Lipton and colleagues found lower levels of fractional anisotropy in parieto–occipital areas which was associated with decreased scores in one of six cognitive tests (poorer memory) and was inversely correlated with the annual number of headers [34].”
BackgroundYuh, E. L., Hawryluk, G. W. J., & Manley, G. T. (2014) · Neurosurgery · doi:10.1227/neu.0000000000000491 · Cited by 72
White matter alterations in college football players: a longitudinal diffusion tensor imaging study
Mayinger, M. C., Merchant‐Borna, K., Hufschmidt, J., Muehlmann, M., Weir, I. R., Rauchmann, B., Shenton, M. E., Koerte, I. K., & Bazarian, J. J. (2017) · Brain Imaging and Behavior · doi:10.1007/s11682-017-9672-4 · Cited by 73
Effects of Repetitive Head Impacts on a Concussion Assessment Battery
Caccese, J. B., Best, C. L., Lamond, L. C., DiFabio, M., Kaminski, T. W., WATSON, D., Getchell, N., & Buckley, T. A. (2019) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001905 · Cited by 66
“It should be noted, however, that we used exclusively clinical concussion assessments whereas neuroimaging approaches have suggested subclinical changes in neurological function in response to RHI in FB, ice hockey, and soccer (11,12,14,17,18), though the clinical significance and the causation of these neuroimaging c…”
BackgroundResultSchneider, D. K., Galloway, R. T., Bazarian, J. J., Diekfuss, J. A., Dudley, J. A., Leach, J. L., Mannix, R., Talavage, T. M., Yuan, W., & Myer, G. D. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2019.6398 · Cited by 65
Practice type effects on head impact in collegiate football
Reynolds, B. B., Patrie, J., Henry, E. J., Goodkin, H. P., Broshek, D. K., Wintermark, M., & Druzgal, T. J. (2016) · Journal of neurosurgery · doi:10.3171/2015.5.jns15573 · Cited by 61
Bari, S., Svaldi, D. O., Jang, I., Shenk, T. E., Poole, V. N., Lee, T. A., Dydak, U., Rispoli, J. V., Nauman, E. A., & Talavage, T. M. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9861-9 · Cited by 69
Chronic Traumatic Encephalopathy Presenting as Alzheimer’s Disease in a Retired Soccer Player
Grinberg, L. T., Anghinah, R., Nascimento, C. F., Amaro, E., Leite, R. P., Martin, M. D. G. M., Naslavsky, M. S., Takada, L. T., Filho, W. J., Pasqualucci, C. A., et al. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160312 · Cited by 59
“Somestudiesassociateheadingswith structuralbrainchanges[4,6],althoughthisisstilla controversialissuebeyondthescopeofthiswork.”
Animal models of closed-skull, repetitive mild traumatic brain injury
Hoogenboom, W. S., Branch, C. A., & Lipton, M. L. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.02.016 · Cited by 59
“Diffusion-weighted imaging and DTI have the potential to identify grades of tissue damage, to track the evolution of changes, and to provide prognostic markers for clinical outcome (Hulkower, Poliak, Rosenbaum, Zimmerman, & Lipton, 2013).”
BackgroundSelf-citationNeuroimaging in repetitive brain trauma
Ng, T. S. C., Lin, A. P., Koerte, I. K., Pasternak, O., Liao, H. V., Merugumala, S. K., Sylvain Bouix, A., & Shenton, M. E. (2014) · Alzheimer s Research & Therapy · doi:10.1186/alzrt239 · Cited by 66
“With regards to sports-related RBT, Lipton and colleagues [27] found that the amount of ball heading in amateur soccer players was associated with lower FA in temporo-occipital WM, while Bazarian and colleagues [28] showed significantly increased FA and MD in high school athletes experiencing concussion throughout a s…”
Comparative Analysis of Head Impact in Contact and Collision Sports
Reynolds, B. B., Patrie, J. T., Henry, E. J., Goodkin, H. P., Broshek, D. K., Wintermark, M., & Druzgal, T. J. (2016) · Journal of Neurotrauma · doi:10.1089/neu.2015.4308 · Cited by 66
“…a clinical diagnosis of concussion, the hypothesized short-term and long-term effects of repetitive subconcussive head impacts on brain structure 14,15,19,21 and function, 13,15–17 coupled with their proposed role in increasing susceptibility to neurodegenerative disorders, 22,23 suggest that…”
Harriss, A. B., Johnson, A. M., Walton, D. M., & Dickey, J. P. (2019) · Musculoskeletal Science and Practice · doi:10.1016/j.msksp.2019.01.009 · Cited by 57
Virgilio, T. G. D., Ietswaart, M., Wilson, L., Donaldson, D. I., & Hunter, A. M. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2019.00294 · Cited by 62
Stewart, W. F., Kim, N., Ifrah, C., Sliwinski, M. J., Zimmerman, M. E., Kim, M., Lipton, R. B., & Lipton, M. L. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00240 · Cited by 55
“Years of soccer play are associated with neuropsychological (NP) impairment (8–23), abnormal white matter microstructure (8, 24), and structural brain changes (25, 26).”
BackgroundInfluentialSelf-citationHead impact exposure in youth football—Are current interventions hitting the target?
Sandmo, S. B., Andersen, T. E., Koerte, I. K., & Bahr, R. (2019) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.13562 · Cited by 55
Diffusion Imaging of Sport-related Repetitive Head Impacts—A Systematic Review
Koerte, I. K., Wiegand, T. L. T., Bonke, E. M., Kochsiek, J., & Shenton, M. E. (2022) · Neuropsychology Review · doi:10.1007/s11065-022-09566-z · Cited by 61
“With regard to specific dMRI sequences, 10 studies used a voxel size of 2 × 2 × 2 mm3 (Bazarian et al., 2014; Champagne et al., 2019; Churchill et al., 2017; de Souza et al., 2020; Kuzminski et al., 2018; Lefebvre et al., 2021; Lipton et al., 2013; Mayinger et al., 2018; Slobounov et al., 2017; Strauss et al., 2021),…”
BackgroundMethodInfluentialConcussion in soccer: a comprehensive review of the literature
Mooney, J. H., Self, D. M., ReFaey, K., Elsayed, G., Chagoya, G., Bernstock, J. D., & Johnston, J. M. (2020) · Concussion · doi:10.2217/cnc-2020-0004 · Cited by 57
Merchant‐Borna, K., Asselin, P. D., Narayan, D. A., Abar, B. W., Jones, C. M. C., & Bazarian, J. J. (2016) · Annals of Biomedical Engineering · doi:10.1007/s10439-016-1680-9 · Cited by 52
Kuzminski, S. J., Clark, M. D., Fraser, M. A., Haswell, C. C., Morey, R. A., Liu, C., Choudhury, K. R., Guskiewicz, K. M., & Petrella, J. R. (2017) · American Journal of Neuroradiology · doi:10.3174/ajnr.a5489 · Cited by 52
“Expanding to other sports, the burden of heading events in adult soccer athletes has been associated with alterations in white matter diffusion metrics and diminished performance on computerized cognitive assessment.(8,9) Given the evidence linking subconcussive impacts to neurophysiological and neuroanatomic alterati…”
BackgroundNeuro-Ophthalmologic Response to Repetitive Subconcussive Head Impacts
Nowak, M. K., Bevilacqua, Z. W., Ejima, K., Huibregtse, M. E., Chen, Z., Mickleborough, T. D., Newman, S. D., & Kawata, K. (2020) · JAMA Ophthalmology · doi:10.1001/jamaophthalmol.2019.6128 · Cited by 53
Mental health and suicide in former professional soccer players
Russell, E., McCabe, T., Mackay, D., Stewart, K., MacLean, J. A., Pell, J. P., & Stewart, W. B., Jr. (2020) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2020-323315 · Cited by 56
Effects of Sex and Event Type on Head Impact in Collegiate Soccer
Reynolds, B. B., Patrie, J. T., Henry, E. J., Goodkin, H. P., Broshek, D. K., Wintermark, M., & Druzgal, T. J. (2017) · Orthopaedic Journal of Sports Medicine · doi:10.1177/2325967117701708 · Cited by 50
“”(1) In the short term, subconcussion can lead to decreased resistance to concussion,(2,13) impaired cognition,(4) changes in brain functional connectivity,(19,38) and disruption of the brain white matter.(9,25) In the long term, subconcussion may increase risk for neurodegenerative disorders, such as amyotrophic late…”
BackgroundAssociation of Increased Serum S100B Levels With High School Football Subconcussive Head Impacts
Zonner, S. W., Ejima, K., Bevilacqua, Z. W., Huibregtse, M. E., Charleston, C. N., Fulgar, C. C., & Kawata, K. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00327 · Cited by 46
“However, subconcussive impact-dependent dysregulation in neural network has been suggested and replicated in a number of studies (52, 53, 55, 56), supporting our findings that peripheral serological factor such as S100B may be a productive avenue to evaluate for potential astrocyte injury from subconcussive head impac…”
ResultMayer, A. R., Ling, J. M., Dodd, A. B., Meier, T. B., Hanlon, F. M., & Klimaj, S. D. (2017) · Brain Imaging and Behavior · doi:10.1007/s11682-016-9546-1 · Cited by 45
“2014) and history of heading the ball in soccer players (Lipton et al. 2013).”
Oculomotor Response to Cumulative Subconcussive Head Impacts in US High School Football Players
Zonner, S. W., Ejima, K., Fulgar, C. C., Charleston, C. N., Huibregtse, M. E., Bevilacqua, Z. W., & Kawata, K. (2018) · JAMA Ophthalmology · doi:10.1001/jamaophthalmol.2018.6193 · Cited by 45
“During game 10 (9-25) 219 (149-535) 18 495 (10 634-48 421)”
InfluentialJang, I., Chun, I. Y., Brosch, J. R., Bari, S., Zou, Y., Cummiskey, B. R., Lee, T. A., Lycke, R., Poole, V. N., Shenk, T. E., et al. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101930 · Cited by 50
“Thus, some studies (e.g., McAllister et al., 2012; Lipton et al., 2013; Bahrami et al., 2016) may have captured post-season measures at a point when regions with increased FA may have balanced those regions exhibiting decreased FA (e.”
InfluentialSundman, M., Doraiswamy, P. M., & Morey, R. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00334 · Cited by 46
“…the brain consistently show long lasting damage following TBI (Inglese et al., 2005; Salmond et al., 2006; Kraus et al., 2007; Lipton et al., 2008; Miles et al., 2008; Niogi et al., 2008; Little et al., 2010; Cubon et al., 2011; Ljungqvist et al., 2011; Davenport et al., 2012; Taber et al., 2015).”
BackgroundQuantifying Head Impacts in Collegiate Lacrosse
Reynolds, B. B., Patrie, J. T., Henry, E. J., Goodkin, H. P., Broshek, D. K., Wintermark, M., & Druzgal, T. J. (2016) · The American Journal of Sports Medicine · doi:10.1177/0363546516648442 · Cited by 47
“’’(1) Evidence indicates that shortterm changes related to subconcussion include increased susceptibility to subsequent concussion,(2,3,21) decreased cognitive function,(4) altered brain gray matter functional connectivity,(25,43) and changes in brain white matter microstructure.(14,32) Over the long term, subconcussi…”
BackgroundCatenaccio, E., Caccese, J. B., Wakschlag, N., Fleysher, R., Kim, N., Kim, M., Buckley, T. A., Stewart, W. F., Lipton, R. B., Kaminski, T. W., et al. (2016) · Research in Sports Medicine · doi:10.1080/15438627.2016.1234472 · Cited by 43
“Although a version of the questionnaire has been employed to assess longer term exposure (Lipton et al., 2013), because the reporting period in the present study is limited to 2 weeks, we cannot specifically generalize our calibration approach to exposure recall over different time periods.”
BackgroundMethodInfluentialSelf-citationStructural neuroimaging in sport-related concussion.
Bigler, E. (2017) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2017.09.006 · Cited by 43
Oliver, J. M., Anzalone, A. J., & Turner, S. M. (2018) · Sports Medicine · doi:10.1007/s40279-017-0847-3 · Cited by 46
“, soccer) [32, 33] are not immune to damage resulting from subconcussive impacts.”
BackgroundSvaldi, D. O., Joshi, C., McCuen, E. C., Music, J. P., Hannemann, R. E., Leverenz, L. J., Nauman, E. A., & Talavage, T. M. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9983-0 · Cited by 42
Sex differences in mechanisms of head impacts in collegiate soccer athletes
Saunders, T. D., Le, R. K., Breedlove, K. M., Bradney, D. A., & Bowman, T. G. (2020) · Clinical Biomechanics · doi:10.1016/j.clinbiomech.2020.02.003 · Cited by 41
Evaluation of an In-Ear Sensor for Quantifying Head Impacts in Youth Soccer
Sandmo, S. B., McIntosh, A. S., Andersen, T. E., Koerte, I. K., & Bahr, R. (2019) · The American Journal of Sports Medicine · doi:10.1177/0363546519826953 · Cited by 40
“There is evidence of long-term structural and functional brain alterations among soccer players.(4-6,9) Moreover, recent studies suggested a potential effect on cognitive function among children and adolescents during a vulnerable period of brain maturation.”
BackgroundSubject-specific multiscale analysis of concussion: from macroscopic loads to molecular-level damage
Montanino, A., Li, X., Zhou, Z., Zeineh, M., Camarillo, D. B., & Kleiven, S. (2021) · Brain Multiphysics · doi:10.1016/j.brain.2021.100027 · Cited by 39
White matter abnormalities in active elite adult rugby players
Zimmerman, K. A., Laverse, E., Samra, R., Lopez, M. Y., Jolly, A., Bourke, N., Graham, N., Patel, M. C., Hardy, J., Kemp, S. P. T., et al. (2021) · Brain Communications · doi:10.1093/braincomms/fcab133 · Cited by 40
Tsushima, W. T., Geling, O., Arnold, M., & Oshiro, R. S. (2016) · Applied Neuropsychology Child · doi:10.1080/21622965.2015.1052813 · Cited by 39
“Evidence is mounting that these nonconcussive impacts can result in neuropathological changes, as observed early in classic studies of laboratory animals subjected to mild head trauma (Denny-Brown & Russell, 1941) and currently documented in advanced neuroimaging findings (Baugh et al., 2012; Lipton et al., 2013; McAl…”
BackgroundPostural Control Deficits After Repetitive Soccer Heading.
Caccese, J., Buckley, T., Tierney, R., Rose, W., Glutting, J., & Kaminski, T. (2018) · Clinical Journal of Sports Medicine · doi:10.1097/jsm.0000000000000709 · Cited by 38
“The neurological effects of soccer heading may depend on the rate of exposures, the time between exposures, and the vulnerability of individual players.(11) A repetitive soccer heading paradigm was developed to serve as an in vivo model of functional head impact testing in soccer players and allows for precise control…”
BackgroundWhite Matter Changes in Posttraumatic Stress Disorder Following Mild Traumatic Brain Injury
Li, L., Sun, G., Liu, K., Li, M., Li, B., Qian, S., & Yu, L. (2016) · Chinese Medical Journal · doi:10.4103/0366-6999.180518 · Cited by 43
“In addition, it has also been established that most patients with low-level head injury recover fully over time,[23] which may indicate that delayed axonal recovery or axonal regrowth in some extent is possible, as reviewed by Povlishock and Katz.”
BackgroundAlosco, M. L., & Stern, R. A. (2019) · Seminars in Pediatric Neurology · doi:10.1016/j.spen.2019.03.016 · Cited by 41
Heading Frequency and Risk of Cognitive Impairment in Retired Male Professional Soccer Players
Espahbodi, S., Hogervorst, E., Macnab, T.-M. P., Thanoon, A. A., Fernandes, G., Millar, B., Duncan, A., Goodwin, M. V., Batt, M. E., Fuller, C. W., et al. (2023) · JAMA Network Open · doi:10.1001/jamanetworkopen.2023.23822 · Cited by 35
The neurobiological effects of repetitive head impacts in collision sports
Hunter, L. E., Branch, C. A., & Lipton, M. L. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.06.016 · Cited by 45
Self-citationRawlings, S., Takechi, R., & Lavender, A. P. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.09.021 · Cited by 34
Estimating Contact Exposure in Football Using the Head Impact Exposure Estimate
Kerr, Z. Y., Littleton, A. C., Cox, L. M., DeFreese, J. D., Varangis, E. M. L., Lynall, R. C., Schmidt, J. D., Marshall, S. W., & Guskiewicz, K. M. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2014.3666 · Cited by 34
“poorer neurocognitive performance was independent of history of concussion, suggesting that a biological pathway involved repeated heading of the ball.(14) Further research is needed to gain a more complete understanding of the potential negative effects of subconcussive impacts.”
BackgroundIs Heading in Youth Soccer Dangerous Play?
O’Kane, J. W. (2016) · The Physician and Sportsmedicine · doi:10.1080/00913847.2016.1149423 · Cited by 32
“[8] in 2013 found heading at a certain threshold does result in brain injury and impaired function.”
BackgroundBatty, G. D., Frank, P., Kujala, U. M., Sarna, S. J., Valencia‐Hernández, C. A., & Kaprio, J. A. (2023) · EClinicalMedicine · doi:10.1016/j.eclinm.2023.102056 · Cited by 35
“42 Spe-ci fi c mechanisms of risk in boxing and American foot-ball (professionals) are less clear.”
BackgroundSubconcussive impacts and imaging findings over a season of contact sports
Davenport, E. M., Urban, J. E., Mokhtari, F., Lowther, E. L., Horn, J. D. V., Vaughan, C. G., Gioia, G. A., Whitlow, C. T., Stitzel, J. D., & Maldjian, J. A. (2016) · Concussion · doi:10.2217/cnc-2016-0003 · Cited by 31
Metadata
- Authors
- Lipton, M. L., Kim, N., Zimmerman, M. E., Kim, M., Stewart, W. F., Branch, C. A., & Lipton, R. B.
- Affiliations
- Albert Einstein College of Medicine (US)
- Sutter Health (US)
- ORCID
- Venue
- Radiology
- Published
- 2013-09
- Volume
- 268
- Issue
- 3
- Pages
- 850-857
- ISSN
- 0033-8419 (ISSN-L)
- 1527-1315
- PMC
- PMC3750422
- OpenAlex
- W2170100452
- Cited by
- 376
- References
- 30
- Citations by year
- 2026: 20 · 2025: 20 · 2024: 20 · 2023: 30 · 2022: 30 · 2021: 30 · 2020: 47 · 2019: 40 · 2018: 37 · 2017: 27 · 2016: 36 · 2015: 15 · 2014: 18 · 2013: 5
- FWCI
- 17.97
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Radiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Dana Foundation
- Yeshiva University
- National Institutes of Health (5k23ns051409-02, 5r01ag025119-05, K23NS05140901A1, AG03949, RO1AG025119, RO1AG12101, PO1 AG03949, PO1AG027734)
- Albert Einstein College of Medicine, Yeshiva University
- National Institute on Aging (R01-AG025119, R01AG022374, P01AG03949, P01AG027734, P01AG003949, R01AG034119, R01AG012101, K23AG030857, R01-AG-12101)
- National Institute of Neurological Disorders and Stroke (K23NS047256, R01NS082432, K23 NS47256, K23NS051409-01A1)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports injuries and prevention
- Keywords
- soccer heading, white matter microstructure, fractional anisotropy, diffusion tensor imaging, cognitive performance, memory, amateur football players, concussion
- MeSH terms
- Adult, Brain Injuries, Cognition Disorders, Female, Humans, Magnetic Resonance Imaging, Male, Nerve Fibers, Myelinated, Sensitivity and Specificity, Soccer, Wounds, Nonpenetrating, Reproducibility of Results
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