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Framing potential for adverse effects of repetitive subconcussive impacts in soccer in the context of athlete and non-athlete controls

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Abstract

The benefits of athletic activity may be attenuated by sport-related head impacts, including soccer-related concussion and subconcussive events. The purpose of this study is to characterize the specific effects of soccer heading on white matter microstructure and cognitive function, independent of concussion, relative to non-athlete controls and relative to active athletes who are not involved in collision sports. 246 amateur soccer players, 72 non-contact/non-collision sports athletes and 110 healthy,non-athlete controls were included in the study, and underwent cognitive testing and 3T diffusion tensor imaging (DTI). Voxelwise linear regression, comparing soccer players and non-contact/non-collision sports athletes healthy,non-athlete controls, identified regions of abnormally low and high fractional anisotropy (FA), axial diffusivity (AD), radial diffusivity (RD) and mean diffusivity (MD) in athlete participants. Generalized estimating equations were used to examine the effects of 2 week and 1 year heading exposure quartile on cognitive performance and on the volume of each high and each low DTI parameter. Athletes with no or lower exposure to repetitive heading exhibited greater expression of low RD, greater expression of high FA and better performance on tasks of attention, processing speed, verbal memory, and working memory compared to non-athletes. Soccer players with the highest exposure to repetitive head impacts, however, did not differ significantly from healthy, non-athletes on either micro-structural features or cognitive performance, findings not explained by concussion history or demographic factors. These results are consistent with the notion that beneficial effects of athletic conditioning or training on brain structure and function may be attenuated by exposure to repeated subconcussive head impacts.

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Funding

This study was funded by the National Institutes of Health (R01NS082432) and the Dana Foundation.

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Correspondence to Michael L. Lipton.

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Conflict of Interest

Sara B. Strauss declares that she has no conflict of interest.

Roman Fleysher declares that he has no conflict of interest.

Chloe Ifrah declares that she has no conflict of interest.

Liane Hunter declares that she has no conflict of interest.

Kenny Ye declares that he has no conflict of interest.

Richard Lipton receives research support from the NIH: 2PO1 AG003949 (mPI), 5U10 NS077308 (PI), RO1 NS082432 (Investigator), 1RF1 AG057531 (Site PI), RF1 AG054548 (Investigator), 1RO1 AG048642 (Investigator), R56 AG057548 (Investigator), K23 NS09610 (Mentor), K23AG049466 (Mentor), 1K01AG054700 (Mentor). He also receives support from the Migraine Research Foundation and the National Headache Foundation. He serves on the editorial board of Neurology, senior advisor to Headache, and associate editor to Cephalalgia. He has reviewed for the NIA and NINDS, holds stock options in eNeura Therapeutics and Biohaven Holdings; serves as consultant, advisory board member, or has received honoraria from: American Academy of Neurology, Alder, Allergan, American Headache Society, Amgen, Autonomic Technologies, Avanir, Biohaven, Biovision, Boston Scientific, Dr. Reddy’s, Electrocore, Eli Lilly, eNeura Therapeutics, GlaxoSmithKline, Merck, Pernix, Pfizer, Supernus, Teva, Trigemina, Vector, Vedanta. He receives royalties from Wolff’s Headache 7th and 8th Edition, Oxford University Press, 2009, Wiley and Informa.

Molly Zimmerman declares that she has no conflict of interest.

Mimi Kim does consulting for Celgene and Eli Lilly on clinical trials, unrelated to the work in the paper.

Walter Stewart declares that he has no conflict of interest.

Michael L. Lipton receives research funding from the National Institutes of Health (R01NS082432), the Dana Foundation and Guerbet and royalties from Springer.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Strauss, S.B., Fleysher, R., Ifrah, C. et al. Framing potential for adverse effects of repetitive subconcussive impacts in soccer in the context of athlete and non-athlete controls. Brain Imaging and Behavior 15, 882–895 (2021). https://doi.org/10.1007/s11682-020-00297-4

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