Soccer Heading Is Associated with White Matter Microstructural and Cognitive Abnormalities
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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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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.
“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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Cites
The assessment and analysis of handedness: The Edinburgh inventory
Oldfield, R. C. (1971) · Neuropsychologia · doi:10.1016/0028-3932(71)90067-4 · Cited by 35,900 · see citing works
(1998) · The Journal of Clinical Psychiatry · Cited by 19,139 · see citing works
Mixed-Effects Models in Sand S-PLUS
Pinheiro, J. C., & Bates, D. M. (2000) · Statistics and Computing · doi:10.1007/978-1-4419-0318-1 · Cited by 11,187 · see citing works
(1998) · PubMed · Cited by 10,216 · see citing works
Statistical parametric maps in functional imaging: A general linear approach
Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J. ‐., Frith, C. D., & Frackowiak, R. S. J. (1994) · Human Brain Mapping · doi:10.1002/hbm.460020402 · Cited by 9,688 · see citing works
Mixed-Effects Models in S and S-PLUS
(2001) · Technometrics · doi:10.1198/tech.2001.s574 · Cited by 9,278 · see citing works
The mini international neuropsychiatric interview
Lecrubier, Y., Sheehan, D. V., Hergueta, T., & Weiller, E. (1998) · European Psychiatry · doi:10.1016/s0924-9338(99)80239-9 · Cited by 5,882 · see citing works
Chronic traumatic encephalopathy in athletes: Progressive tauopathy after repetitive head injury
McKee, A. C., Cantu, R. C., Nowinski, C. J., Hedley-Whyte, E. T., Gavett, B. E., Budson, A. E., Santini, V. E., Lee, H.-S., Kubilus, C. A., & Stern, R. A. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181a9d503 · Cited by 2,295 · see citing works
Robust regression using iteratively reweighted least-squares.
Holland, P. W., & Welsch, R. E. (1977) · Communications in Statistics - Theory and Methods · doi:10.1080/03610927708827533 · Cited by 2,115 · see citing works
Nonlinear Mixed Effects Models for Repeated Measures Data
Lindstrom, M. J., & Bates, D. M. (1990) · Biometrics · doi:10.2307/2532087 · Cited by 1,793 · see citing works
MARTLAND, H. S. (1928) · Journal of the American Medical Association · doi:10.1001/jama.1928.02700150029009 · Cited by 774 · see citing works
Update of Neuropathology and Neurological Recovery After Traumatic Brain Injury
Povlishock, J. T., & Katz, D. I. (2005) · Journal of Head Trauma Rehabilitation · doi:10.1097/00001199-200501000-00008 · Cited by 676 · see citing works
Maruff, P., Thomas, E., Cysique, L., Brew, B., Collie, A., Snyder, P., & Pietrzak, R. H. (2009) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/acp010 · Cited by 635 · see citing works
Traumatic Brain Injury in High School Athletes
Powell, J. W. (1999) · JAMA · doi:10.1001/jama.282.10.958 · Cited by 587 · see citing works
Smith, S. M., Johansen‐Berg, H., Jenkinson, M., Rueckert, D., Nichols, T. E., Miller, K. L., Robson, M. D., Jones, D. K., Klein, J. C., Bartsch, A. J., et al. (2007) · Nature Protocols · doi:10.1038/nprot.2007.45 · Cited by 578 · see citing works
Collie, A., Maruff, P. T., Darby, D., & McStephen, M. (2003) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617703930074 · Cited by 455 · see citing works
Neuropsychological Impairment in Amateur Soccer Players
Matser, E. J. T. (1999) · JAMA · doi:10.1001/jama.282.10.971 · Cited by 400 · see citing works
Diffusion Tensor Imaging of Mild Traumatic Brain Injury
Niogi, S. N., & Mukherjee, P. (2010) · Journal of Head Trauma Rehabilitation · doi:10.1097/htr.0b013e3181e52c2a · Cited by 380 · see citing works
Chronic traumatic brain injury in professional soccer players
Matser, J. T., Kessels, A. G. H., Jordan, B. D., Lezak, M. D., & Troost, J. (1998) · Neurology · doi:10.1212/wnl.51.3.791 · Cited by 319 · see citing works
Lipton, M. L., Gulko, E., Zimmerman, M. E., Friedman, B. W., Kim, M., Gellella, E., Gold, T., Shifteh, K., Ardekani, B. A., & Branch, C. A. (2009) · Radiology · doi:10.1148/radiol.2523081584 · Cited by 291 · see citing works
Self-citationWhite Matter Integrity in the Brains of Professional Soccer Players Without a Symptomatic Concussion
Koerte, I. K., Ertl-Wagner, B. B., Reiser, M. F., ZAFONTE, R. D., & Shenton, M. E. (2012) · JAMA · doi:10.1001/jama.2012.13735 · Cited by 245 · see citing works
Gysland, S. M., Mihalik, J. P., Register-Mihalik, J. K., Trulock, S. C., Shields, E. W., & Guskiewicz, K. M. (2012) · Annals of Biomedical Engineering · doi:10.1007/s10439-011-0421-3 · Cited by 189 · see citing works
Palacios, E. M., Sala‐Llonch, R., Junqué, C., Fernández‐Espejo, D., Roig-Rovira, T., Tormos, J. M., Bargalló, N., & Vendrell, P. (2012) · Cortex · doi:10.1016/j.cortex.2012.02.011 · Cited by 142 · see citing works
Koutures, C. G., & Gregory, A. J. M. (2010) · PEDIATRICS · doi:10.1542/peds.2009-3009 · Cited by 107 · see citing works
Spiotta, A. M., Bartsch, A., & Benzel, E. C. (2011) · Neurosurgery · doi:10.1227/neu.0b013e31823021b2 · Cited by 107 · see citing works
The Neuropsychology of Heading and Head Trauma in Association Football (Soccer): A Review
Rutherford, A., Stephens, R. J., & Potter, D. D. (2003) · Neuropsychology Review · doi:10.1023/a:1025525613477 · Cited by 84 · see citing works
Prevention of arm injury in youth baseball pitchers.
Kerut, E. K., Kerut, D. G., Fleisig, G. S., & Andrews, J. R. (2008) · PubMed · Cited by 64 · see citing works
Stephens, R., Rutherford, A., Potter, D. D., & Fernie, G. (2005) · Child Neuropsychology: A Journal of Normal and Abnormal Development in Childhood and Adolescence · doi:10.1080/092970490959629 · Cited by 55 · see citing works
Subconcussive Impact in Sports: A New Era of Awareness
Spiotta, A. M., Shin, J. H., Bartsch, A., & Benzel, E. C. (2011) · World Neurosurgery · doi:10.1016/j.wneu.2011.01.019 · Cited by 51 · see citing works
Patlak, M., Joy, J. E., Institute of Medicine (U.S.), & IOM Workshop on Neuropsychological Consequences of Head Impact in Sports <2001, W. (2002) · Cited by 3 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [1]Martland HS. Punch drunk. JAMA 1928;91(15):1103–1107 [Google Scholar]
- [22]Fox J, Weisberg S. An R companion to applied regression. 2nd ed. Los Angeles, Calif: Sage, 2011 [Google Scholar]
Cited by
Sorted by citations
The New Neurometabolic Cascade of Concussion
Giza, C. C., & Hovda, D. A. (2014) · Neurosurgery · doi:10.1227/neu.0000000000000505 · Cited by 1,353 · see citing works
A systematic review of potential long-term effects of sport-related concussion.
Manley, G., Gardner, A. J., Schneider, K. J., Guskiewicz, K. M., Bailes, J., Cantu, R. C., Castellani, R. J., Turner, M., Jordan, B. D., Randolph, C., et al. (2017) · British Journal of Sports Medicine · doi:10.1136/bjsports-2017-097791 · Cited by 663 · see citing works
Montenigro, P., Alosco, M., Martin, B. M., Daneshvar, D., Mez, J., Chaisson, C. E., Nowinski, C., Au, R., Mckee, A., Cantu, R., et al. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2016.4413 · Cited by 535 · see citing works
Military-related traumatic brain injury and neurodegeneration
McKee, A. C., & Robinson, M. E. (2014) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2014.04.003 · Cited by 423 · see citing works
McKee, A. C., Daneshvar, D. H., Alvarez, V. E., & Stein, T. D. (2014) · Acta Neuropathologica · doi:10.1007/s00401-013-1230-6 · Cited by 422 · see citing works
Ling, H., Morris, H. R., Neal, J. W., Lees, A. J., Hardy, J., Holton, J. L., Revesz, T., & Williams, D. D. R. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1680-3 · Cited by 252 · see citing works
Neurological consequences of traumatic brain injuries in sports
Ling, H., Hardy, J., & Zetterberg, H. (2015) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2015.03.012 · Cited by 197 · see citing works
Subconcussive head impacts in sport: A systematic review of the evidence
Mainwaring, L. M., Pennock, K. F., Mylabathula, S., & Alavie, B. Z. (2018) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2018.01.007 · Cited by 189 · see citing works
Evidence for Acute Electrophysiological and Cognitive Changes Following Routine Soccer Heading
Virgilio, T. G. D., Hunter, A. M., Wilson, L., Stewart, W. B., Jr., Goodall, S., Howatson, G., Donaldson, D. I., & Ietswaart, M. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.10.029 · Cited by 175 · see citing works
Asken, 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 · see citing works
Neuroimaging Biomarkers in Mild Traumatic Brain Injury (mTBI)
Bigler, E. D. (2013) · Neuropsychology Review · doi:10.1007/s11065-013-9237-2 · Cited by 166 · see citing works
Russell, E., Mackay, D., Stewart, K., MacLean, J. A., Pell, J. P., & Stewart, W. B., Jr. (2021) · JAMA Neurology · doi:10.1001/jamaneurol.2021.2403 · Cited by 158 · see citing works
McKee, A. C., Mez, J., Abdolmohammadi, B., Butler, M. L. M. D., Huber, B. R., Uretsky, M., Babcock, K. J., Cherry, J. D., Alvarez, V. E., Martin, B. M., et al. (2023) · JAMA Neurology · doi:10.1001/jamaneurol.2023.2907 · Cited by 166 · see citing works
Altered 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 158 · see citing works
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 · see citing works
A review of neuroimaging findings in repetitive brain trauma
Koerte, I. K., Lin, A. P., Willems, A., Muehlmann, M., Hufschmidt, J., Coleman, M. J., Green, I., Liao, H., Tate, D. F., Wilde, E. A., et al. (2015) · Brain Pathology · doi:10.1111/bpa.12249 · Cited by 160 · see citing works
Cortical 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 · see citing works
White 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 126 · see citing works
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 126 · see citing works
Tarnutzer, A. A., Straumann, D., Brugger, P., & Feddermann‐Demont, N. (2016) · British Journal of Sports Medicine · doi:10.1136/bjsports-2016-096593 · Cited by 119 · see citing works
Gutierrez, G. M., Conte, C., & Lightbourne, K. (2014) · Pediatric Exercise Science · doi:10.1123/pes.2013-0102 · Cited by 116 · see citing works
Murugavel, M., Cubon, V. A., Putukian, M., Echemendía, R. J., Cabrera, J., Osherson, D. N., & Dettwiler, A. (2014) · Journal of Neurotrauma · doi:10.1089/neu.2014.3368 · Cited by 113 · see citing works
Rosenkrantz, A. B., Ayoola, A., Singh, K., & Duszak, R. (2017) · Academic Radiology · doi:10.1016/j.acra.2016.11.019 · Cited by 114 · see citing works
Lamond, L. C., Caccese, J. B., Buckley, T. A., Glutting, J. J., & Kaminski, T. W. (2018) · Journal of Athletic Training · doi:10.4085/1062-6050-90-17 · Cited by 105 · see citing works
Traumatic 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 105 · see citing works
Noble, J. M., & Hesdorffer, D. C. (2013) · Neuropsychology Review · doi:10.1007/s11065-013-9239-0 · Cited by 103 · see citing works
Alosco, M. L., Tripodis, Y., Jarnagin, J., Baugh, C. M., Martin, B. M., Chaisson, C. E., Estochen, N., Song, L., Cantu, R. C., Jeromin, A., et al. (2016) · Alzheimer s & Dementia Diagnosis Assessment & Disease Monitoring · doi:10.1016/j.dadm.2016.11.003 · Cited by 100 · see citing works
Use 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 · see citing works
Sasaki, T., Pasternak, O., Mayinger, M. C., Muehlmann, M., Savadjiev, P., Sylvain Bouix, A., Kubicki, M. R., Fredman, E., Dahlben, B., Helmer, K. G., et al. (2014) · Journal of neurosurgery · doi:10.3171/2013.12.jns132092 · Cited by 96 · see citing works
Impaired Cognitive Performance in Youth Athletes Exposed to Repetitive Head Impacts
Koerte, I. K., Nichols, E., Tripodis, Y., Schultz, V., Lehner, S., Igbinoba, R., Chuang, A. Z., Mayinger, M. C., Klier, E. M., Muehlmann, M., et al. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2016.4960 · Cited by 94 · see citing works
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 · see citing works
Levitch, C. F., Zimmerman, M. E., Lubin, N., Kim, N., Lipton, R. B., Stewart, W. F., Kim, M., & Lipton, M. L. (2017) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617717000790 · Cited by 85 · see citing works
Self-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 · see citing works
Moore, R. D., Lepine, J., & Dave Ellemberg, A. (2016) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2016.11.011 · Cited by 81 · see citing works
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 · see citing works
Concussion—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 79 · see citing works
Jones, S. V., Breakey, R. W. F., & Evans, P. J. (2013) · British Journal of Sports Medicine · doi:10.1136/bjsports-2013-092758 · Cited by 82 · see citing works
Biomechanical Perspectives on Concussion in Sport
Rowson, S., Bland, M. L., Campolettano, E., Press, J. N., Rowson, B., Smith, J. A., Sproule, D. W., Tyson, A. M., & Duma, S. (2016) · Sports medicine and arthroscopy review · doi:10.1097/jsa.0000000000000121 · Cited by 83 · see citing works
Sugarman, M. A., McKee, A. C., Stein, T. D., Tripodis, Y., Besser, L. M., Martin, B. M., Palmisano, J. N., Steinberg, E. G., O’Connor, M. K., Au, R., et al. (2019) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2018.12.015 · Cited by 75 · see citing works
Advanced biomarkers of pediatric mild traumatic brain injury: Progress and perils
Mayer, A. R., Kaushal, M., Dodd, A. B., Hanlon, F. M., Shaff, N. A., Mannix, R., Master, C. L., Leddy, J. J., Stephenson, D. D., Wertz, C. J., et al. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.08.002 · Cited by 74 · see citing works
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 · see citing works
Self-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 · see citing works
Minimizing 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 · see citing works
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 · see citing works
Caccese, J. B., Lamond, L. C., Buckley, T. A., & Kaminski, T. W. (2016) · Research in Sports Medicine · doi:10.1080/15438627.2016.1230549 · Cited by 74 · see citing works
Heading 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 · see citing works
Association 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 · see citing works
Potential for use of creatine supplementation following mild traumatic brain injury
Ainsley Dean, P. J., Arikan, G., Opitz, B., & Sterr, A. (2017) · Concussion · doi:10.2217/cnc-2016-0016 · Cited by 67 · see citing works
Hallock, H., Mantwill, M., Vajkoczy, P., Wolfarth, B., Reinsberger, C., Lampit, A., & Finke, C. (2023) · Neurology Clinical Practice · doi:10.1212/cpj.0000000000200123 · Cited by 73 · see citing works
Symptoms from repeated intentional and unintentional head impact in soccer players
Stewart, W. F., Kim, N., Ifrah, C., Lipton, R. B., Bachrach, T. A., Zimmerman, M. E., Kim, M., & Lipton, M. L. (2017) · Neurology · doi:10.1212/wnl.0000000000003657 · Cited by 69 · see citing works
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 · see citing works
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 · see citing works
Beaudouin, 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 · see citing works
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 · see citing works
Yuh, E. L., Hawryluk, G. W. J., & Manley, G. T. (2014) · Neurosurgery · doi:10.1227/neu.0000000000000491 · Cited by 66 · see citing works
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 66 · see citing works
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 · see citing works
Schneider, 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 · see citing works
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 · see citing works
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 62 · see citing works
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 · see citing works
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 57 · see citing works
Self-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 58 · see citing works
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 57 · see citing works
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 · see citing works
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 57 · see citing works
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 · see citing works
Self-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 · see citing works
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 56 · see citing works
Concussion 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 · see citing works
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 · see citing works
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 · see citing works
Neuro-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 50 · see citing works
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 53 · see citing works
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 48 · see citing works
Association 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 47 · see citing works
Mayer, 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 · see citing works
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 · see citing works
Jang, 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 45 · see citing works
Sundman, M., Doraiswamy, P. M., & Morey, R. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00334 · Cited by 43 · see citing works
Quantifying 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 43 · see citing works
Catenaccio, 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 · see citing works
Self-citationStructural neuroimaging in sport-related concussion
Bigler, E. D. (2017) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2017.09.006 · Cited by 43 · see citing works
Oliver, J. M., Anzalone, A. J., & Turner, S. M. (2018) · Sports Medicine · doi:10.1007/s40279-017-0847-3 · Cited by 44 · see citing works
Svaldi, 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 · see citing works
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 · see citing works
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 · see citing works
Subject-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 38 · see citing works
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 · see citing works
Tsushima, W. T., Geling, O., Arnold, M., & Oshiro, R. S. (2016) · Applied Neuropsychology Child · doi:10.1080/21622965.2015.1052813 · Cited by 39 · see citing works
Postural 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 · see citing works
White 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 37 · see citing works
Alosco, M. L., & Stern, R. A. (2019) · Seminars in Pediatric Neurology · doi:10.1016/j.spen.2019.03.016 · Cited by 37 · see citing works
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 · see citing works
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 35 · see citing works
Self-citationRawlings, S., Takechi, R., & Lavender, A. P. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.09.021 · Cited by 34 · see citing works
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 · see citing works
Is Heading in Youth Soccer Dangerous Play?
O’Kane, J. W. (2016) · The Physician and Sportsmedicine · doi:10.1080/00913847.2016.1149423 · Cited by 32 · see citing works
Batty, 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 32 · see citing works
Subconcussive 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 · see citing works
- 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 › Epidemiology › 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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