Cited by 376Traumatic Brain Injury ResearchAdvanced Neuroimaging Techniques and ApplicationsSports injuries and prevention

The DOI matches its Crossref record; 30 of the 30 references it cites were found in a registry or an index.

Soccer Heading Is Associated with White Matter Microstructural and Cognitive Abnormalities

Open access

Lipton, Michael L., Kim, Namhee, Zimmerman, Molly E., Kim, Mimi, Stewart, Walter F., Branch, Craig A., Lipton, Richard B.·2013·Radiology

DOI 10.1148/radiol.13130545PMC PMC3750422

Open this paper in CoChat — free account

Abstract

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1148/radiol.13130545

Cites

30 of 30 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

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
Untitled work
(1998) · The Journal of Clinical Psychiatry · Cited by 19,139
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
Untitled work
(1998) · PubMed · Cited by 10,216
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
Mixed-Effects Models in S and S-PLUS
(2001) · Technometrics · doi:10.1198/tech.2001.s574 · Cited by 9,278
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 5,899
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
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
Nonlinear Mixed Effects Models for Repeated Measures Data
Lindstrom, M. J., & Bates, D. M. (1990) · Biometrics · doi:10.2307/2532087 · Cited by 1,793

Flagged first, then by citations

Show all 30 references

Research works printed but not linked: 2

Sheehan DV, 1998, J Clin Psychiatry, 59, 22
Kerut EK, 2008, J La State Med Soc, 160, 95

Sorted by citations

Items 101–200 of 375

Parents’ intentions to allow youth football participation: Perceived concussion risk and the theory of planned behavior.
Murphy, A. M., Askew, K. L., & Sumner, K. E. (2017) · Sport Exercise and Performance Psychology · doi:10.1037/spy0000102 · Cited by 31
“While soccer is often seen as a safer alternative to football in terms of concussion risk (Cantu, 2012), it is among the riskiest (Levy et al., 2012)—with high rates of concussion (Gessel et al., 2007) and research supporting potential long-term brain changes from head contact (Lipton et al., 2013).”
Background
Framing potential for adverse effects of repetitive subconcussive impacts in soccer in the context of athlete and non-athlete controls
Strauß, S., Fleysher, R., Ifrah, C., Hunter, L. E., Ye, K. Q., Lipton, R. B., Zimmerman, M. E., Kim, M., Stewart, W. F., & Lipton, M. L. (2020) · Brain Imaging and Behavior · doi:10.1007/s11682-020-00297-4 · Cited by 31
Self-citation
Direct player observation is needed to accurately quantify heading frequency in youth soccer
Harriss, A. B., Walton, D. M., & Dickey, J. P. (2018) · Research in Sports Medicine · doi:10.1080/15438627.2018.1431534 · Cited by 31
“Player self-report methods offer a more a convenient way to quantify the number of headers performed, and have been used to identify whether long-term exposure to heading results in adverse neurological outcomes (Lipton et al., 2013; Straume-Naesheim, Andersen, Dvorak, & Bahr, 2005).”
BackgroundResultInfluential
Management of concussion in soccer
Hubertus, V., Marklund, N., & Vajkoczy, P. (2019) · Acta Neurochirurgica · doi:10.1007/s00701-019-03807-6 · Cited by 28
The long-term consequences of repetitive head impacts: Chronic traumatic encephalopathy
Alosco, M. L., & Stern, R. A. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-12-804766-8.00018-2 · Cited by 28
Characterization of On-Field Head Impact Exposure in Youth Soccer
Tomblin, B. T., Pritchard, N. S., Filben, T. M., Miller, L. E., Miles, C. M., Urban, J. E., & Stitzel, J. D. (2020) · Journal of Applied Biomechanics · doi:10.1123/jab.2020-0071 · Cited by 27
The role of diffusion tensor imaging in characterizing injury patterns on athletes with concussion and subconcussive injury: a systematic review
Tayebi, M., Holdsworth, S. J., Champagne, A. A., Cook, D. J., Nielsen, P. M. F., Lee, T., Wang, A., Fernandez, J., & Shim, V. (2021) · Brain Injury · doi:10.1080/02699052.2021.1895313 · Cited by 26
“Future directions The discrepancies observed in various studies highlighted the need for new analysis techniques to support the DTI findings such as myelin water imaging (95), diffusion basis spectrum imaging (96), neurite orientation dispersion and density imaging (NODDI)(68), diffusion kurtosis imaging (DKI) (36,72,…”
Background
Characterization of Head Impact Exposure in Women’s Collegiate Soccer
Filben, T. M., Pritchard, N. S., Miller, L. E., Woods, S. K., Hayden, M. E., Miles, C. M., Urban, J. E., & Stitzel, J. D. (2021) · Journal of Applied Biomechanics · doi:10.1123/jab.2020-0304 · Cited by 27
Multimodal MR Imaging Signatures of Cognitive Impairment in Active Professional Fighters
Mishra, V. R., Zhuang, X., Sreenivasan, K. R., Banks, S. J., Yang, Z., Bernick, C. B., & Cordes, D. (2017) · Radiology · doi:10.1148/radiol.2017162403 · Cited by 27
Susceptibility-Weighted Imaging and Magnetic Resonance Spectroscopy in Concussion
Kirov, I. I., Whitlow, C. T., & Zamora, C. A. (2017) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2017.09.007 · Cited by 26
Impairment of cerebrovascular reactivity in response to hypercapnic challenge in a mouse model of repetitive mild traumatic brain injury
Lynch, C., Eisenbaum, M., Algamal, M., Balbi, M., Ferguson, S., Mouzon, B., Saltiel, N. A., Ojo, J. O., Diaz-Arrastia, R. R., Mullan, M., et al. (2020) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x20954015 · Cited by 25
Neurocognitive performance and mental health of retired female football players compared to non-contact sport athletes
Prien, A., Feddermann‐Demont, N., Verhagen, E. A. L. M., Twisk, J. W. R., & Junge, A. (2020) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2020-000952 · Cited by 30
Automated soccer head impact exposure tracking using video and deep learning
Rezaei, A., & Wu, L. C. (2022) · Scientific Reports · doi:10.1038/s41598-022-13220-2 · Cited by 30
“For players that self-reported long-term exposure of 885 to 1800 headers per year, brain white matter microstructure abnormality and neurocognitive dysfunction has been found 8 .”
Background
Examining Neurocognitive Function in Previously Concussed Interscholastic Female Soccer Players
Forbes, C., Glutting, J. J., & Kaminski, T. W. (2014) · Applied Neuropsychology Child · doi:10.1080/21622965.2014.933108 · Cited by 25
“Realizing that this is an imaging study and that heading frequency was selfreported, the results nonetheless are interesting in that they relate the changes to heading frequency and not concussion history (Lipton et al., 2013).”
Background
Health problems in former elite female football players: Prevalence and risk factors
Prien, A., Prinz, B., Dvořák, J., & Junge, A. (2016) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.12747 · Cited by 25
Mild Jugular Compression Collar Ameliorated Changes in Brain Activation of Working Memory after One Soccer Season in Female High School Athletes
Yuan, W., Dudley, J. A., Foss, K. D. B., Ellis, J. D., Thomas, S. M., Galloway, R. T., DiCesare, C. A., Leach, J. L., Adams, J. M., Maloney, T., et al. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2017.5262 · Cited by 26
“Additional factors, such as menstrual cycle/estrogen level 61 and heading statistics, 67 may need to beevaluatedinfuturestudies.”
Emerging advances of in vivo detection of chronic traumatic encephalopathy and traumatic brain injury
Dallmeier, J., Meysami, S., Merrill, D. A., & Raji, C. A. (2019) · British Journal of Radiology · doi:10.1259/bjr.20180925 · Cited by 25
Associations of Apolipoprotein E ε4 Genotype and Ball Heading With Verbal Memory in Amateur Soccer Players
Hunter, L. E., Freudenberg‐Hua, Y., Davies, P., Kim, M., Lipton, R. B., Stewart, W. F., Srinivasan, P., Hu, S., & Lipton, M. L. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2019.4828 · Cited by 26
“Years playing soccer at similar frequency, median (IQR)a 11 (7-16) 10 (5-16) 12 (8-18) 11 (7-15) .”
BackgroundMethodSelf-citation
Heading in the Right Direction: A Critical Review of Studies Examining the Effects of Heading in Soccer Players
Snowden, T. M., Reid, H. M. O., Kennedy, S., Kenny, R., McQuarrie, A. M., Stuart-Hill, L. A., García-Barrera, M. A., Gawryluk, J. R., & Christie, B. R. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7130 · Cited by 25
“8,11 In addition, players with the highest lifetime estimates of heading exposure were found to score lower in measures of attention, concentration, cognitive ﬂexibility, and general intellectual functioning compared with counterparts with low heading exposure.”
Sex as a Biological Variable in Preclinical Modeling of Blast-Related Traumatic Brain Injury
McCabe, J. T., & Tucker, L. B. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.541050 · Cited by 24
Immediate effects of an acute bout of repeated soccer heading on cognitive performance
Ashton, J. S., Coyles, G., Malone, J. J., & Roberts, J. W. (2020) · Science and Medicine in Football · doi:10.1080/24733938.2020.1846769 · Cited by 24
“Many previous studies involve a retrospective battery of neuropsychological tests, where players are sometimes arbitrarily categorised by their chronic incidence of heading before finally being tested long after the incidence itself (Tysvaer 1992; Lipton et al. 2013).”
Background
Neuroimaging of Concussion
Honce, J. M., Nyberg, E. M., Jones, I., & Nagae, L. M. (2016) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/j.pmr.2016.01.002 · Cited by 28
Effects of a 6-Week Strength Training of the Neck Flexors and Extensors on the Head Acceleration during Headers in Soccer.
Becker, S. T., Berger, J., Backfisch, M., Ludwig, O., Kelm, J., & Fröhlich, M. (2019) · PubMed Central · Cited by 24
Comparison of women’s collegiate soccer header kinematics by play state, intent, and outcome
Filben, T. M., Pritchard, N. S., Hanes-Romano, K., Miller, L. E., Miles, C. M., Urban, J. E., & Stitzel, J. D. (2021) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2021.110619 · Cited by 23
The Role of Virtual Reality in the Management of Football Injuries
Demeco, A., Salerno, A., Gusai, M., Vignali, B., Gramigna, V., Palumbo, A., Corradi, A., Mickeviciute, G., & Costantino, C. (2024) · Medicina · doi:10.3390/medicina60061000 · Cited by 25
Chronic traumatic encephalopathy: neuroimaging biomarkers
Lin, A. P., Charney, M. F., Shenton, M. E., & Koerte, I. K. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63954-7.00029-x · Cited by 25
Gender differences in anthropometric parameters and technical performance of youth soccer players
Perroni, F., Gallotta, M. C., Pisano, S., Reis, V. M., Emerenziani, G. P., Guidetti, L., & Baldari, C. (2018) · Sport Sciences for Health · doi:10.1007/s11332-018-0456-z · Cited by 22
“Amateur soccer athletes self-reporting between 276 and 1096 headers per year [46].”
Background
Analytical modelling of soccer heading
Taha, Z., Hassan, M. H. A., & Hasanuddin, I. (2015) · Sadhana · doi:10.1007/s12046-015-0383-5 · Cited by 22
Chronic Traumatic Encephalopathy and Other Long-term Sequelae
Jordan, B. D. (2014) · CONTINUUM Lifelong Learning in Neurology · doi:10.1212/01.con.0000458972.94013.e1 · Cited by 22
“Lipton and colleagues observed reduced fractional anisotropy in temporo-occipital white matter of amateur soccer players, which correlated with poorer memory scores and frequency of heading.(38) This association was not accountable by a history of concussion.”
Background
Preliminary evidence from a prospective DTI study suggests a posterior‐to‐anterior pattern of recovery in college athletes with sports‐related concussion
Cubon, V. A., Murugavel, M., Holmes, K. W., & Dettwiler, A. (2018) · Brain and Behavior · doi:10.1002/brb3.1165 · Cited by 22
Functional, Structural, and Neurotoxicity Biomarkers in Integrative Assessment of Concussions
Dambinova, S. A., Maroon, J. C., Sufrinko, A. M., Mullins, J. D., Alexandrova, E. V., & Aa, P. (2016) · Frontiers in Neurology · doi:10.3389/fneur.2016.00172 · Cited by 21
“Overall, data from DTI studies of mTBI have been contradictory, however, showing both increased FA values in acute and chronic studies (57, 58) as well as decreased FA levels (59).”
Background
In-Game Head Impact Exposure of Male and Female High School Soccer Players
Nevins, D. D., Hildenbrand, K. J., Vasavada, A. N., Kensrud, J., & Smith, L. V. (2018) · Athletic Training & Sports Health Care · doi:10.3928/19425864-20180802-02 · Cited by 23
No Evidence of Association Between Soccer Heading and Cognitive Performance in Professional Soccer Players: Cross-Sectional Results
Rodrigues, A. C., Lima, M. D. M., de Souza, L. C., Furtado, C., Marques, C. E., Gonçalves, L. I., de Lima, M. V. A., Lasmar, R. C. P., & Caramelli, P. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00209 · Cited by 21
“Also, heading technique may vary among soccer players (5), resulting in situations of greater or lesser risk for head injury, a variable that was not controlled for in our study.”
Background
Neurocognitive performance and symptom profiles of Spanish-speaking Hispanic athletes on the ImPACT test.
Ott, S., Schatz, P., Solomon, G., & Ryan, J. J. (2014) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/act091 · Cited by 26
Neck and Trunk Strength Training to Mitigate Head Acceleration in Youth Soccer Players
Müller, C., & Zentgraf, K. (2020) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000003822 · Cited by 20
ADHD May Associate With Reduced Tolerance to Acute Subconcussive Head Impacts: A Pilot Case-Control Intervention Study
Nowak, M. K., Ejima, K., Quinn, P. D., Bazarian, J. J., Mickleborough, T. D., Harezlak, J., Newman, S. D., & Kawata, K. (2020) · Journal of Attention Disorders · doi:10.1177/1087054720969977 · Cited by 20
“, 2017), increase axonal diffusion (Hirad et al., 2019; Lipton et al., 2013), impair ocular-motor function (Kawata, Rubin, et al.”
Background
Evolving concepts of chronic traumatic encephalopathy as a neuropathological entity
Ling, H., Neal, J., & Révész, T. (2017) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12425 · Cited by 19
The brains of elite soccer players are subject to experience-dependent alterations in white matter connectivity
Yao, Z., Sligte, I. G., Moreau, D., Hsieh, S., Yang, C.-T., Ridderinkhof, K. R., Muggleton, N. G., & Wang, C. (2020) · Cortex · doi:10.1016/j.cortex.2020.07.016 · Cited by 21
Blood–brain barrier disruption and ventricular enlargement are the earliest neuropathological changes in rats with repeated sub-concussive impacts over 2 weeks
Hiles-Murison, B., Lavender, A. P., Hackett, M. J., Armstrong, J. J., Nesbit, M., Rawlings, S., McGonigle, T., Warnock, A., Lam, V., Mamo, J. C. L., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-88854-9 · Cited by 19
REPIMPACT - a prospective longitudinal multisite study on the effects of repetitive head impacts in youth soccer
Koerte, I. K., Bahr, R., Filipčík, P., Gooijers, J., Leemans, A., Lin, A. P., Tripodis, Y., Shenton, M. E., Sochen, N., Swinnen, S. P., et al. (2021) · Brain Imaging and Behavior · doi:10.1007/s11682-021-00484-x · Cited by 19
Comparing fMRI activation during smooth pursuit eye movements among contact sport athletes, non-contact sport athletes, and non-athletes
Kellar, D., Newman, S., Pestilli, F., Cheng, H., & Port, N. (2018) · NeuroImage: Clinical · doi:10.1016/j.nicl.2018.01.025 · Cited by 21
“More recently, numerous MRI studies have been conducted on subconcussion, including using diffusion imaging and the diffusion tensor model (DTI), which looks for damage in the white matter (Bahrami et al., 2016; Bazarian et al., 2014; Chappell et al., 2008, 2006; Davenport et al., 2016, 2014; Helmer et al., 2014; Koer…”
Background
Association Between Proteomic Blood Biomarkers and DTI/NODDI Metrics in Adolescent Football Players: A Pilot Study
Kawata, K., Steinfeldt, J. A., Huibregtse, M. E., Nowak, M. K., Macy, J. T., Kercher, K. A., Rettke, D. J., Shin, A., Chen, Z., Ejima, K., et al. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.581781 · Cited by 19
“Furthermore, the immature (teenage) brain has shown to exhibit more pronounced axonal diffusion in the corpus callosum and longitudinal fasciculus (50, 51) following repetitive subconcussive head impacts compared to the mature brain (52), given that neural networks in the frontal cortex proliferate throughout adolesce…”
Background
Neuroimaging and Neuropsychological Studies in Sports-Related Concussions in Adolescents: Current State and Future Directions
Narayana, S., Charles, C., Collins, K. L., Tsao, J. W., Stanfill, A. G., & Baughman, B. C. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00538 · Cited by 23
“Many of these fractional anisotropy changes are localized to the temporo-occipital white matter (60), but deep white matter changes may show an even longer time course of recovery, especially for female athletes.”
Background
Soccer heading and concussion are not associated with reduced brain volume or cortical thickness
Oliveira, T. G., Ifrah, C., Fleysher, R., Stockman, M., & Lipton, M. L. (2020) · PLoS ONE · doi:10.1371/journal.pone.0235609 · Cited by 18
“Indeed, imaging studies have identified adverse microstructural effects of heading, suggestive of traumatic axonal injury [5, 8].”
BackgroundInfluentialSelf-citation
Head impacts in semiprofessional male Soccer players: a prospective video analysis over one season of competitive games
Cassoudesalle, H., Bildet, M., Petit, H., & Dehail, P. (2020) · Brain Injury · doi:10.1080/02699052.2020.1831067 · Cited by 18
Assessment of Neuropsychological Function in Veterans With Blast-Related Mild Traumatic Brain Injury and Subconcussive Blast Exposure
Clausen, A. N., Bouchard, H. C., Workgroup, V. M.-A. M., Welsh-Bohmer, K. A., & Morey, R. A. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.686330 · Cited by 18
Heading and risk of injury situations for the head in professional German football: a video analysis of over 150,000 headers in 110,000 match minutes
Weber, J., Reinsberger, C., Krutsch, V., Seiffert, R., Huber, L., Alt, V., & Krutsch, W. (2022) · Science and Medicine in Football · doi:10.1080/24733938.2022.2114602 · Cited by 18
“Recent studies have indicated that heading in football may be dangerous for the brain because of changes to its micro-structure and neurochemistry and effecting neurocognitive changes (Koerte et al. 2012, 2015; Haran et al. 2013; Lipton et al. 2013; Di Virgilio et al. 2016; Mackay et al. 2019).”
Background
Soccer heading immediately alters brain function and brain-muscle communication
Parr, J. V. V., Uiga, L., Marshall, B., & Wood, G. (2023) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2023.1145700 · Cited by 21
“, 2017), a finding that becomes concerning given amateur soccer players may be exposed to thousands of heading impacts per year (Lipton et al., 2013).”
Background
Altered Functional and Structural Connectomes in Female High School Soccer Athletes After a Season of Head Impact Exposure and the Effect of a Novel Collar
Dudley, J. A., Yuan, W., Diekfuss, J. A., Foss, K. D. B., DiCesare, C. A., Altaye, M., Logan, K., Leach, J. L., & Myer, G. D. (2020) · Brain Connectivity · doi:10.1089/brain.2019.0729 · Cited by 18
“…microstructural integrity of white matter (Bahrami et al., 2016; Bazarian et al., 2014; Chun et al., 2015; Churchill et al., 2017; Davenport et al., 2014; Lipton et al., 2013; Mayinger et al., 2018; McAllister et al., 2014; Myer et al., 2016a,b, 2019; Schneider et al., 2019; Yuan et al., 2018a).”
Validation of HeadCount-2w for estimation of two-week heading: Comparison to daily reporting in adult amateur player
Lipton, M. L., Ifrah, C., Stewart, W. F., Fleysher, R., Sliwinski, M. J., Kim, M., & Lipton, R. B. (2017) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2017.08.008 · Cited by 18
Self-citation
Increased Myo-Inositol in Primary Motor Cortex of Contact Sports Athletes without a History of Concussion
Lefebvre, G., Chamard, É., Proulx, S., Tremblay, S., Halko, M. A., Soman, S., de Guise, É., Pascual‐Leone, Á., & Théoret, H. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2017.5254 · Cited by 17
Proceedings from the Ice Hockey Summit III: Action on Concussion
Smith, A. M., Alford, P. W., Aubry, M., Benson, B. W., Black, A. M., Brooks, A., Burke, C. J., D’Arcy, R. C. N., Dodick, D. W., Eaves, M., et al. (2019) · Current Sports Medicine Reports · doi:10.1249/jsr.0000000000000557 · Cited by 17
Effects of purposeful soccer heading on circulating small extracellular vesicle concentration and cargo
Muñoz, E. R., Caccese, J. B., Wilson, B. E., Shuler, K. T., dos Santos, F. V., Cabán, C. T., Jeka, J. J., Langford, D., & Hudson, M. B. (2020) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2020.11.006 · Cited by 17
“, functional magnetic resonance imaging and diffusion tensor imaging) can identify functional impairments and changes in white matter microstructure but requires expensive equipment and advanced training.(5,6) In this context, other more sensitive and specific markers for acute and chronic changes are needed.”
Background
Long-Term Anesthetic-Dependent Hypoactivity after Repetitive Mild Traumatic Brain Injuries in Adolescent Mice
Semple, B. D., Sadjadi, R., Carlson, J., Chen, Y., Xu, D., Ferriero, D. M., & Noble‐Haeusslein, L. J. (2016) · Developmental Neuroscience · doi:10.1159/000448089 · Cited by 17
Systematic Review of the Long-Term Neuroimaging Correlates of Mild Traumatic Brain Injury and Repetitive Head Injuries
Echlin, H. V., Rahimi, A., & Wojtowicz, M. A. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.726425 · Cited by 16
Neurocognitive Performance of 425 Top-Level Football Players: Sport-specific Norm Values and Implications
Prien, A., Junge, A., Brugger, P., Straumann, D., & Feddermann‐Demont, N. (2018) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/acy056 · Cited by 16
Soccer heading and subclinical neuropsychiatric symptomatology in professional soccer players
Amitay, N., Zlotnik, Y., Coreanu, T., Zeller, L., Abu‐Salameh, I., Novack, V., & Ifergane, G. (2020) · Neurology · doi:10.1212/wnl.0000000000010244 · Cited by 16
Changes in resting‐state functional brain connectivity associated with head impacts over one men’s semi‐professional soccer season
Cassoudesalle, H., Petit, A., Chanraud, S., Petit, H., Badaut, J., Sibon, I., & Dehail, P. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24742 · Cited by 16
“Analyzing video recordings of the games is considered the gold standard for quantifying repetitive head impacts in soccer (Harriss et al., 2018), more reliable than the self-questionnaires usually used in the rare neuroimaging studies in soccer players (Koerte et al., 2016; Lipton et al., 2013).”
Background
Ball heading and subclinical concussion in soccer as a risk factor for anterior cruciate ligament injury
Kakavas, G., Malliaropoulos, N., Błach, W., Bikos, G. D., Migliorini, F., & Maffulli, N. (2021) · Journal of Orthopaedic Surgery and Research · doi:10.1186/s13018-021-02711-z · Cited by 16
Effects of soccer ball inflation pressure and velocity on peak linear and rotational accelerations of ball-to-head impacts
Cecchi, N. J., Monroe, D. C., Moscoso, W. X., Hicks, J. W., & Reinkensmeyer, D. J. (2020) · Sports Engineering · doi:10.1007/s12283-020-00331-0 · Cited by 16
Pilot characterization of head kinematics in grassroots dirt track racing
Filben, T. M., Pritchard, N. S., Oravec, C. S., Hile, C. W., Bercaw, J. R., Zoch, S. R., Miller, L. E., Bullock, G. S., Flashman, L. A., Miles, C. M., et al. (2022) · Traffic Injury Prevention · doi:10.1080/15389588.2022.2103688 · Cited by 15
“Previous research in soccer has reported neurological deficits among players who experienced a high frequency of heading (i.e., greater than 885–1800 headers per year) (Lipton et al. 2013).”
Background
Age of first exposure to soccer heading: Associations with cognitive, clinical, and imaging outcomes in the Einstein Soccer Study
Charney, M. F., Ye, K. Q., Fleysher, R., DeMessie, B., Stewart, W. F., Zimmerman, M. E., Kim, M., Lipton, R. B., & Lipton, M. L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1042707 · Cited by 15
“In a 2013 study of a non-overlapping sample of soccer players, adverse effects on cognition and brain microstructure were found above a threshold level of cumulative heading exposure (26).”
BackgroundSelf-citation
Sport-Related Traumatic Brain Injury with and without Helmets in Children
Bandte, A., Fritzsche, F. S., Emami, P., Kammler, G., Püschel, K., & Krajewski, K. L. (2017) · World Neurosurgery · doi:10.1016/j.wneu.2017.12.094 · Cited by 15
Evaluating the validity of self-report as a method for quantifying heading exposure in male youth soccer
Sandmo, S. B., Gooijers, J., Seer, C., Kaufmann, D., Bahr, R., Pasternak, O., Lipton, M. L., Tripodis, Y., & Koerte, I. K. (2020) · Research in Sports Medicine · doi:10.1080/15438627.2020.1853541 · Cited by 16
“Moreover, recent evidence also suggests that heading may impair cognitive function in both adults (Lipton et al., 2013; Stewart et al., 2018) and adolescents (Koerte et al., 2017; Zhang et al., 2013).”
BackgroundMethodResultInfluentialSelf-citation
Video analysis of 100 matches in male semi-professional football reveals a heading rate of 5.7 headings per field player and match
Weber, J., Ernstberger, A., Reinsberger, C., Popp, D., Nerlich, M. L., Alt, V., & Krutsch, W. (2022) · BMC Sports Science Medicine and Rehabilitation · doi:10.1186/s13102-022-00521-2 · Cited by 17
Repetitive soccer heading adversely impacts short-term learning among adult women
Ye, K. Q., Fleysher, R., Lipton, R. B., Zimmerman, M. E., Stewart, W. F., Sliwinski, M. J., Kim, M., & Lipton, M. L. (2022) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2022.08.011 · Cited by 15
Self-citation
White matter microstructural abnormalities in blast-exposed combat veterans: accounting for potential pre-injury factors using consanguineous controls
McClelland, A. C., Fleysher, R., Mu, W.-Y., Kim, N., & Lipton, M. (2018) · Neuroradiology · doi:10.1007/s00234-018-2070-9 · Cited by 9
Self-citation
Diffusion Tensor Imaging in Contact and Non-Contact University-Level Sport Athletes
Lefebvre, G., Guay, S., Chamard, É., Theaud, G., de Guise, É., Bacon, B. A., Descoteaux, M., Beaumont, L. D., & Théoret, H. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7170 · Cited by 12
“26,27,31,32 The extent and duration of injury associated with repetitive blows to the head in the absence of concussion are not yet clear, 34 but may have signiﬁcant clinical impact.”
Altered Attention Network in Paratroopers Exposed to Repetitive Subconcussion: Evidence Based on Behavioral and Event-Related Potential Results
Chen, A., Zhang, Z., Cao, C., Lu, J., Wu, S., Ma, S., Feng, Y., Wang, S., Xu, G., & Song, J. (2021) · Journal of Neurotrauma · doi:10.1089/neu.2021.0253 · Cited by 14
The Reliability of Transcranial Magnetic Stimulation-Derived Corticomotor Inhibition as a Brain Health Evaluation Tool in Soccer Players
Virgilio, T. G. D., Ietswaart, M., Selvamoorthy, R., & Hunter, A. M. (2022) · Sports Medicine - Open · doi:10.1186/s40798-021-00399-3 · Cited by 14
“Such injuries have been shown to be associated with both acute and chronic impairments to cognitive function [1–3], motor control [4–6] and brain structure [1, 7].”
Background
Purposeful heading in U.S. youth soccer players: results from the U.S. soccer online heading survey – epidemiological evidence
Kaminski, T. W., Chiampas, G., Putukian, M., Kirkendall, D. T., Fokas, J. A., & Kontos, A. P. (2019) · Science and Medicine in Football · doi:10.1080/24733938.2019.1677937 · Cited by 14
“…the media, parents, and researchers alike have expressed concerns about potential adverse effects associated with purposeful heading including concussion (Maher et al. 2014; Hassan et al. 2018) and repetitive micro-trauma to the brain (Dashnaw et al. 2012; Lipton et al. 2013; Hunter et al. 2018).”
BackgroundResult
CSF and Blood Neurofilament Levels in Athletes Participating in Physical Contact Sports
Verduyn, C., Bjerke, M., Duerinck, J., Engelborghs, S., Peers, K., Versijpt, J. J., & D’haeseleer, M. (2021) · Neurology · doi:10.1212/wnl.0000000000011750 · Cited by 14
“, having a higher number of headings was associated with an augmented burden of neurologic symptoms, both assessed with questionnaires) and radiologic (self-reported number of headings was associated with abnormal white matter microstructure on diffusion tensorMRI) findings also defend the theory that such challenges…”
Background
Short-Term Neurologic Manifestations of Repetitive Head Impacts Among Athletes: A Scoping Review
Stephen, S. J., Hasman, L., Goldenberg, M., Merchant-Borna, K., Kawata, K., Mannix, R., & Bazarian, J. J. (2022) · Journal of Head Trauma Rehabilitation · doi:10.1097/htr.0000000000000767 · Cited by 16
Youth Soccer Parents' Attitudes and Perceptions About Concussions
Kim, S., & Connaughton, D. P. (2020) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2020.04.029 · Cited by 13
Does acute soccer heading cause an increase in plasma S100B? A randomized controlled trial
Huibregtse, M. E., Nowak, M. K., Kim, J. E., Kalbfell, R. M., Koppineni, A., Ejima, K., & Kawata, K. (2020) · PLoS ONE · doi:10.1371/journal.pone.0239507 · Cited by 14
“For example, retrospective questionnaires estimate that a collegiate soccer player performs up to 500 headers during a single season and over 3,000 during the course of a career [9, 10].”
Background
Exploring the Effects of a Neck Strengthening Program on Purposeful Soccer Heading Biomechanics and Neurocognition
Waring, K. M., Smith, E. R., Austin, G. P., & Bowman, T. G. (2022) · International Journal of Sports Physical Therapy · doi:10.26603/001c.38327 · Cited by 12
Purposeful Heading Performed by Female Youth Soccer Players Leads to Strain Development in Deep Brain Structures
Brooks, J. S., Allison, W., Harriss, A. B., Bian, K., Mao, H., & Dickey, J. P. (2021) · Neurotrauma Reports · doi:10.1089/neur.2021.0014 · Cited by 14
“In contrast, one study demonstrated a positive association between the number of headers a soccer player performed in a year to the degree of axonal brain injury.(5) Reduced brain activity(6,7) as well as increases in radial and axial diffusivity(8) are”
Result
Training matters: Heading incidence and characteristics in children's and youth football (soccer) players
Reeschke, R., Haase, F. K., Dautzenberg, L., Krutsch, W., & Reinsberger, C. (2023) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.14408 · Cited by 12
Sensory Reweighting for Upright Stance in Soccer Players: A Comparison of High and Low Exposure to Soccer Heading
Caccese, J. B., dos Santos, F. V., Yamaguchi, F., & Jeka, J. J. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7001 · Cited by 12
“Further, soccer heading exposure was self-reported via the Einstein Heading Questionnaire.13 The accuracy of exposure may be influenced by several factors, including sex and current health status.20 Because participant recall may be biased, we chose to analyze exposure as a binary variable (i.e., high exposure vs. low…”
BackgroundMethodResultInfluential
The Influence of Fatigued Core Muscles on Head Acceleration during Headers in Soccer
Becker, S. T., Fröhlich, M., Kelm, J., & Ludwig, O. (2018) · Sports · doi:10.3390/sports6020033 · Cited by 11
Neuroimaging of brain trauma in sports
Suri, A. K., & Lipton, M. L. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63954-7.00021-5 · Cited by 12
“For example, amateur soccer players show a decline of FA relative to the amount of heading they do, in a dose-dependent fashion (Lipton et al., 2013).”
BackgroundSelf-citation
Use of diffusion tension imaging in the evaluation of pediatric concussions
Satchell, E. K., Friedman, S. D., Bompadre, V., Poliakov, A. V., Oron, A. P., & Jinguji, T. M. (2019) · Musculoskeletal Science and Practice · doi:10.1016/j.msksp.2019.05.002 · Cited by 11
A comprehensive prospective examination of purposeful heading in American interscholastic and collegiate soccer players
Kaminski, T. W., Weinstein, S., & Wahlquist, V. E. (2019) · Science and Medicine in Football · doi:10.1080/24733938.2019.1696470 · Cited by 11
“They suggest that cumulative heading over a one-year period is associated with cognitive dysfunction and multi-structural alteration of white matter determined using advanced MRI technology (Lipton et al. 2013; Levitch et al. 2018).”
Background
The Impact of Sleep on the Relationship between Soccer Heading Exposure and Neuropsychological Function in College-Age Soccer Players
Levitch, C. F., McConathey, E. M., Aghvinian, M. N., Himmelstein, M., Lipton, M. L., & Zimmerman, M. E. (2020) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617720000211 · Cited by 11
“The HeadCount questionnaires (Catenaccio et al., 2016; Lipton et al., 2017; Lipton et al., 2013; Stewart et al., 2017) and PSQI (Carpenter & Andrykowski, 1998; Mollayeva et al., 2016) have demonstrated reliability and validity across settings but caution should still be taken when interpreting the…”
BackgroundResultInfluentialSelf-citation
[Inferior vena cava thrombosis responsible for chronic Budd-Chiari syndrome during hepatic and digestive amyloidosis].
Paliard, P., Bretagnolle, M., Collet, P. H., Vannieuwenhyse, A., & Berger, F. (1983) · PubMed · Cited by 11
Altered Vestibular Balance Function in Combat Sport Athletes
Banman, C. J., Schneider, K., Cluff, T., & Peters, R. M. (2021) · Journal of Neurotrauma · doi:10.1089/neu.2020.7432 · Cited by 11
In-Season Concussion Symptom Reporting in Male and Female Collegiate Rugby Athletes
Kieffer, E. E., Brolinson, P. G., Maerlender, A. E., Smith, E. P., & Rowson, S. (2021) · Neurotrauma Reports · doi:10.1089/neur.2021.0050 · Cited by 11
Football and Dementia: Understanding the Link
Neal, J., Hutchings, P. B., Phelps, C., & Williams, D. D. R. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.849876 · Cited by 10
“Exposure to heading over a 12-month duration found impaired memory and attention (59) and accorded with results of MRI performed over a 1-year period with adult soccer players after heading which demonstrated white matter micro-structural changes and contemporaneous poor memory scores (60).”
Result
Heading and unintentional head impacts have opposing associations with Patient Reported Outcomes in amateur soccer players
Hunter, L. E., Ifrah, C., Zimmerman, M. E., Kim, M., Lipton, R. B., Stewart, W. F., & Lipton, M. L. (2018) · Research in Sports Medicine · doi:10.1080/15438627.2018.1492396 · Cited by 10
“We have recently shown that repetitive sub-concussive impacts due to heading are associated with worse cognition (Levitch et al., 2017; Lipton et al., 2013; Stewart et al., in press) and that both heading and unintentional head impacts (e.g. head to head or head to goalpost) can produce CNS…”
BackgroundResultInfluentialSelf-citation
Unifying Pathophysiological Explanations for Sports-Related Concussion and Concussion Protocol Management: Literature Review
Satarasinghe, P., Hamilton, D. K., Buchanan, R. J., & Koltz, M. T. (2019) · Journal of Experimental Neuroscience · doi:10.1177/1179069518824125 · Cited by 10
Finite Element Analysis of Soccer Heading
Hassan, M. H. A., & Taha, Z. (2015) · Procedia Engineering · doi:10.1016/j.proeng.2015.07.174 · Cited by 10
Update
Jones, N. S. (2014) · Current Sports Medicine Reports · doi:10.1249/jsr.0000000000000085 · Cited by 9
“would increase the risk of concussion greatly (31).”
Background
Head Impact Characteristics Based on Player Position in Collegiate Soccer Athletes
Katelyn, N., Daidone, E. H. K., Breedlove, K. M., Bradney, D. A., & Bowman, T. G. (2020) · International Journal of Athletic Therapy & Training · doi:10.1123/ijatt.2019-0095 · Cited by 9
Head impacts in Canadian varsity football: an exploratory study
Corbin‐Berrigan, L., Wagnac, É., Vinet, S.-A., Charlebois‐Plante, C., Guay, S., & Beaumont, L. D. (2021) · Concussion · doi:10.2217/cnc-2020-0024 · Cited by 9
Assessing the association between on-field heading technique and head impact kinematics in a cohort of female youth soccer players
Filben, T. M., Tomblin, B. T., Pritchard, N. S., Bullock, G. S., Hemmen, J. M., Neri, K. E., Krug, V., Miles, C. M., Stitzel, J. D., & Urban, J. E. (2023) · Science and Medicine in Football · doi:10.1080/24733938.2023.2264272 · Cited by 10
“…effects of heading exposure over shorter periods of time (e.g., acute bouts of heading, single seasons) have been mixed (Kaminski et al. 2007, 2008; Lipton et al. 2013; Kawata et al. 2016; DiVirgilio et al. 2016; Hwang et al. 2017; Wallace et al. 2018; Wirsching et al. 2019; Gallagher et al. 2020;…”
Evolving brain and behaviour changes in rats following repetitive subconcussive head impacts
Hoogenboom, W. S., Rubin, T. G., Ambadipudi, K., Cui, M., Ye, K. Q., Foster, H., Elkouby, E., Liu, J., Branch, C. A., & Lipton, M. L. (2023) · Brain Communications · doi:10.1093/braincomms/fcad316 · Cited by 10
“6 Low FA is consistent with microstructural pathology due to RSHI, although an interaction between stress and RSHI should be a focus of further investigation.”
BackgroundSelf-citation
Should heading be forbidden in children’s football?
Tarnutzer, A. A. (2017) · Science and Medicine in Football · doi:10.1080/24733938.2017.1386793 · Cited by 9
“Since then many studies have followed, some of them confirmed early findings (Downs and Abwender 2002; Witol and Webbe 2003; Lipton et al. 2013), others refuted them (Kaminski et al. 2007; Rutherford et al. 2009; Stephens et al. 2010).”
BackgroundResultInfluential
A Prospective Transcranial Doppler Ultrasound-Based Evaluation of the Effects of Repetitive Subconcussive Head Trauma on Neurovascular Coupling Dynamics
Wright, A. D., Smirl, J. D., Bryk, K. N., Jakovac, M., & van Donkelaar, P. (2018) · Clinical Journal of Sport Medicine · doi:10.1097/jsm.0000000000000578 · Cited by 9
A pilot study of diffusion tensor imaging metrics and cognitive performance pre and post repetitive, intentional sub-concussive heading in soccer practice
Kenny, R., Mayo, C. D., Kennedy, S., Varga, A. A., Stuart-Hill, L. A., García-Barrera, M. A., McQuarrie, A. M., Christie, B. R., & Gawryluk, J. R. (2019) · Journal of Concussion · doi:10.1177/2059700219885503 · Cited by 9
“Congruently, results from a landmark study by Lipton et al.(23) revealed that short-term high-frequency heading was associated with lower FA in temporal and occipital regions.”
BackgroundMethodResultInfluential
Age of First Exposure to Soccer Heading and Sensory Reweighting for Upright Stance
Caccese, J. B., dos Santos, F. V., Yamaguchi, F., & Jeka, J. J. (2020) · International Journal of Sports Medicine · doi:10.1055/a-1141-3553 · Cited by 9

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: Lipton, Michael L.
Kim, Namhee
Zimmerman, Molly E.
Kim, Mimi
Stewart, Walter F.
Branch, Craig A.
Lipton, Richard B.
Venue: Radiology
Publisher: Radiological Society of North America (RSNA)
Published: 2013-09
Volume: 268
Issue: 3
Pages: 850-857
ISSN: 0033-8419 (ISSN-L)
1527-1315
DOI: 10.1148/radiol.13130545
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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Soccer Heading Is Associated with White Matter Microstructural and Cognitive Abnormalities

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks