Accumulation of high magnitude acceleration events predicts cerebrovascular reactivity changes in female high school soccer athletes
Mitigating the effects of repetitive exposure to head trauma has become a major concern for the general population, given the growing body of evidence that even asymptomatic exposure to head accelerations is linked with increased risk for negative life outcomes and that risk increases as exposure is prolonged over many years. Among women's sports, soccer currently exhibits the highest growth in participation and reports the largest number of mild traumatic brain injuries annually, making female soccer athletes a relevant population in assessing the effects of repetitive exposure to head trauma. Cerebrovascular biomarkers may be useful in assessing the effects of repetitive head trauma, as these are thought to contribute directly to neurocognitive symptoms associated with mild traumatic brain injury. Here we use fMRI paired with a hypercapnic breath hold task along with monitoring of head acceleration events, to assess the relationship between cerebrovascular brain changes and exposure to repetitive head trauma over a season of play in female high school soccer athletes. We identified longitudinal changes in cerebrovascular reactivity that were significantly associated with prolonged accumulation to high magnitude (> 75th percentile) head acceleration events. Findings argue for active monitoring of athletes during periods of exposure to head acceleration events, illustrate the importance of collecting baseline (i.e., pre-exposure) measurements, and suggest modeling as a means of guiding policy to mitigate the effects of repetitive head trauma.
KeywordsCerebrovascular Reactivity Functional magnetic resonance imaging Concussion Mild traumatic brain injury Subconcussive injury Soccer
This work was funded in part by support from the BrainScope Company, as part of a grant obtained from the GE-NFL Head Health Initiative, and by General Electric Healthcare.
This study was funded in part by the Indiana Clinical and Translational Sciences Institute Spinal Cord and Brain Injury Research Fund (Grant #SCBI 207–32), and the BrainScope Company (as part of a grant from the GE-NFL Head Health Initiative).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the Purdue Institutional Review Board and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all participants of 18 years and above, and parental consent and participant assent were obtained for all participants under the age of 18.
- Abbas, K., Shenk, T. E., Poole, V. N., Breedlove, E. L., Leverenz, L. J., Nauman, E. A., et al. (2015a). Alteration of default mode network in high school football athletes due to repetitive subconcussive mild traumatic brain injury: a resting-state functional magnetic resonance imaging study. Brain Connectivity, 5(2), 91–101. https://doi.org/10.1089/brain.2014.0279.CrossRefPubMedGoogle Scholar
- Abbas, K., Shenk, T. E., Poole, V. N., Robinson, M. E., Leverenz, L. J., Nauman, E. A., et al. (2015b). Effects of repetitive subconcussive brain injury on the functional connectivity of Default Mode Network in high school football athletes. Developmental Neuropsychology, 40(1), 51–56. https://doi.org/10.1080/87565641.2014.990455.CrossRefPubMedGoogle Scholar
- Bahrami, N., Sharma, D., Rosenthal, S., Davenport, E. M., Urban, J. E., Wagner, B., et al. (2016). Subconcussive Head Impact Exposure and White Matter Tract Changes over a Single Season of Youth Football. Radiology, 281(3), 919–926. https://doi.org/10.1148/radiol.2016160564.CrossRefPubMedPubMedCentralGoogle Scholar
- Bari, S., Svaldi, D. O., Jang, I., Shenk, T., Poole, V. N., Lee, T., et al. (2018). Dependence on subconcussive impacts of brain metabolism in collision sport athletes: an MR spectroscopic study. Brain Imaging and Behavior. https://doi.org/10.1007/s11682-018-9861-9.
- Bartnik-Olson, B. L., Holshouser, B., Wang, H., Grube, M., Tong, K., Wong, V., et al. (2014). Impaired neurovascular unit function contributes to persistent symptoms after concussion: a pilot study. Journal of Neurotrauma, 31(17), 1497–1506. https://doi.org/10.1089/neu.2013.3213.CrossRefPubMedGoogle Scholar
- Bazarian, J. J., Zhu, T., Zhong, J., Janigro, D., Rozen, E., Roberts, A., et al. (2014). Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts. [Observational Study Research Support, Non-U.S. Gov't]. PLoS One, 9(4), e94734. https://doi.org/10.1371/journal.pone.0094734.CrossRefPubMedPubMedCentralGoogle Scholar
- Breedlove, E. L., Robinson, M., Talavage, T. M., Morigaki, K. E., Yoruk, U., O'Keefe, K., et al. (2012). Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.]. Journal of Biomechanics, 45(7), 1265–1272. https://doi.org/10.1016/j.jbiomech.2012.01.034.CrossRefPubMedGoogle Scholar
- Chan, S. T., Evans, K. C., Rosen, B. R., Song, T. Y., & Kwong, K. K. (2015). A case study of magnetic resonance imaging of cerebrovascular reactivity: a powerful imaging marker for mild traumatic brain injury. Brain Injury, 29(3), 403–407. https://doi.org/10.3109/02699052.2014.974209.CrossRefPubMedGoogle Scholar
- Chun, I. Y., Mao, X., Breedlove, E. L., Leverenz, L. J., Nauman, E. A., & Talavage, T. M. (2015). DTI Detection of Longitudinal WM Abnormalities Due to Accumulated Head Impacts. [Research Support, Non-U.S. Gov't]. Developmental Neuropsychology, 40(2), 92–97. https://doi.org/10.1080/87565641.2015.1020945.CrossRefPubMedGoogle Scholar
- Cummiskey, B., Schiffmiller, D., Talavage, T. M., Leverenz, L., Meyer, J. J., Adams, D., et al. (2017). Reliability and accuracy of helmet-mounted and head-mounted devices used to measure head accelerations. Proceedings of the Institution of Mechanical Engineers, Part P: Journal of Sports Engineering and Technology, 231(2), 144–153. https://doi.org/10.1177/1754337116658395.CrossRefGoogle Scholar
- Davenport, E. M., Apkarian, K., Whitlow, C. T., Urban, J. E., Jensen, J. H., Szuch, E., et al. (2016). Abnormalities in Diffusional Kurtosis Metrics Related to Head Impact Exposure in a Season of High School Varsity Football. Journal of Neurotrauma, 33(23), 2133–2146. https://doi.org/10.1089/neu.2015.4267.CrossRefPubMedPubMedCentralGoogle Scholar
- Davenport, E. M., Whitlow, C. T., Urban, J. E., Espeland, M. A., Jung, Y., Rosenbaum, D. A., et al. (2014). Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. [Research Support, N.I.H., Extramural]. Journal of Neurotrauma, 31(19), 1617–1624. https://doi.org/10.1089/neu.2013.3233.CrossRefPubMedPubMedCentralGoogle Scholar
- Ellis, M. J., Ryner, L. N., Sobczyk, O., Fierstra, J., Mikulis, D. J., Fisher, J. A., et al. (2016). Neuroimaging Assessment of Cerebrovascular Reactivity in Concussion: Current Concepts, Methodological Considerations, and Review of the Literature. Frontiers in Neurology, 7, 61. https://doi.org/10.3389/fneur.2016.00061.CrossRefPubMedPubMedCentralGoogle Scholar
- Johnson, B., Neuberger, T., Gay, M., Hallett, M., & Slobounov, S. (2014). Effects of subconcussive head trauma on the default mode network of the brain. [Research Support, Non-U.S. Gov't]. Journal of Neurotrauma, 31(23), 1907–1913. https://doi.org/10.1089/neu.2014.3415.CrossRefPubMedPubMedCentralGoogle Scholar
- Len, T. K., Neary, J. P., Asmundson, G. J., Candow, D. G., Goodman, D. G., Bjornson, B., et al. (2013). Serial monitoring of CO2 reactivity following sport concussion using hypocapnia and hypercapnia. Brain Injury, 27(3), 346–353. https://doi.org/10.3109/02699052.2012.743185.CrossRefPubMedGoogle Scholar
- Lewis, P. M., Czosnyka, M., Smielewski, P., & Pickard, J. D. (2014). Cerebrovascular Autoregulation and Monitoring of Cerebrovascular Reactivity. In E. H. Lo, M. Ning, J. Lok, & M. J. Whalen (Eds.), Vascular Mechanisms in CNS and Trauma. New York: Springer.Google Scholar
- McAllister, T. W., Ford, J. C., Flashman, L. A., Maerlender, A., Greenwald, R. M., Beckwith, J. G., et al. (2014). Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology, 82(1), 63–69. https://doi.org/10.1212/01.wnl.0000438220.16190.42.CrossRefPubMedPubMedCentralGoogle Scholar
- Montenigro, P. H., Alosco, M. L., Martin, B. M., Daneshvar, D. H., Mez, J., Chaisson, C. E., et al. (2017). Cumulative Head Impact Exposure Predicts Later-Life Depression, Apathy, Executive Dysfunction, and Cognitive Impairment in Former High School and College Football Players. Journal of Neurotrauma, 34(2), 328–340. https://doi.org/10.1089/neu.2016.4413.CrossRefPubMedPubMedCentralGoogle Scholar
- Morris, B. (2015). Why Is the U.S. So Good at Women's Soccer? http://fivethirtyeight.com/datalab/why-is-the-u-s-so-good-at-womens-soccer/.
- Mutch, W. A., Ellis, M. J., Ryner, L. N., Ruth Graham, M., Dufault, B., Gregson, B., et al. (2016). Brain magnetic resonance imaging CO2 stress testing in adolescent postconcussion syndrome. Journal of Neurosurgery, 125(3), 648–660. https://doi.org/10.3171/2015.6.JNS15972.CrossRefPubMedGoogle Scholar
- Poole, V. N., Abbas, K., Shenk, T. E., Breedlove, E. L., Breedlove, K. M., Robinson, M. E., et al. (2014). MR spectroscopic evidence of brain injury in the non-diagnosed collision sport athlete. Developmental Neuropsychology, 39(6), 459–473. https://doi.org/10.1080/87565641.2014.940619.CrossRefPubMedGoogle Scholar
- Poole, V. N., Breedlove, E. L., Shenk, T. E., Abbas, K., Robinson, M. E., Leverenz, L. J., et al. (2015). Subconcussive hit characteristics predict deviant brain metabolism in football athletes. Developmental Neuropsychology, 40(1), 12–17. https://doi.org/10.1080/87565641.2014.984810.CrossRefPubMedGoogle Scholar
- Robinson, M. E., Shenk, T. E., Breedlove, E. L., Leverenz, L. J., Nauman, E. A., & Talavage, T. M. (2015). The role of location of subconcussive head impacts in FMRI brain activation change. Developmental Neuropsychology, 40(2), 74–79. https://doi.org/10.1080/87565641.2015.1012204.CrossRefPubMedGoogle Scholar
- Schultz, V., Stern, R. A., Tripodis, Y., Stamm, J. M., Wrobel, P., Lepage, C., et al. (2017). Age at First Exposure to Repetitive Head Impacts Is Associated with Smaller Thalamic Volumes in Former Professional American Football Players. Journal of Neurotrauma. https://doi.org/10.1089/neu.2017.5145.CrossRefGoogle Scholar
- Slobounov, S. M., Walter, A., Breiter, H. C., Zhu, D. C., Bai, X., Bream, T., et al. (2017). The effect of repetitive subconcussive collisions on brain integrity in collegiate football players over a single football season: A multi-modal neuroimaging study. Neuroimage Clin, 14, 708–718. https://doi.org/10.1016/j.nicl.2017.03.006.CrossRefPubMedPubMedCentralGoogle Scholar
- Stamm, J. M., Koerte, I. K., Muehlmann, M., Pasternak, O., Bourlas, A. P., Baugh, C. M., et al. (2015). Age at First Exposure to Football is Associated with Altered Corpus Callosum White Matter Microstructure in Former Professional Football Players. Journal of Neurotrauma. https://doi.org/10.1089/neu.2014.3822.CrossRefGoogle Scholar
- Svaldi, D. O., Joshi, C., Robinson, M. E., Shenk, T. E., Abbas, K., Nauman, E. A., et al. (2015). Cerebrovascular reactivity alterations in asymptomatic high school football players. Developmental Neuropsychology, 40(2), 80–84. https://doi.org/10.1080/87565641.2014.973959.CrossRefPubMedGoogle Scholar
- Svaldi, D. O., McCuen, E. C., Joshi, C., Robinson, M. E., Nho, Y., Hannemann, R., et al. (2017). Cerebrovascular reactivity changes in asymptomatic female athletes attributable to high school soccer participation. Brain Imaging and Behavior, 11(1), 98–112. https://doi.org/10.1007/s11682-016-9509-6.CrossRefPubMedGoogle Scholar
- Tagge, C. A., Fisher, A. M., Minaeva, O. V., Gaudreau-Balderrama, A., Moncaster, J. A., Zhang, X.-L., et al. (2018). Concussion, microvascular injury, and early tauopathy in young athletes after impact head injury and an impact concussion mouse model. Brain, awx350-awx350. https://doi.org/10.1093/brain/awx350.CrossRefGoogle Scholar
- Talavage, T. M., Nauman, E. A., Breedlove, E. L., Yoruk, U., Dye, A. E., Morigaki, K. E., et al. (2014). Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. Journal of Neurotrauma, 31(4), 327–338. https://doi.org/10.1089/neu.2010.1512.CrossRefPubMedPubMedCentralGoogle Scholar