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Accumulation of high magnitude acceleration events predicts cerebrovascular reactivity changes in female high school soccer athletes

  • Diana O. Svaldi
  • Chetas Joshi
  • Emily C. McCuen
  • Jacob P. Music
  • Robert Hannemann
  • Larry J. Leverenz
  • Eric A. Nauman
  • Thomas M. Talavage
Original Research

Abstract

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.

Keywords

Cerebrovascular Reactivity Functional magnetic resonance imaging Concussion Mild traumatic brain injury Subconcussive injury Soccer 

Notes

Acknowledgments

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.

Funding

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.

Ethical approval

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

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.

Supplementary material

11682_2018_9983_MOESM1_ESM.eps (12.6 mb)
Fig. S1 Distributions of estimated nCPTA coefficient \( \left({\widehat{x}}_{1, Th,j}\right) \) at each follow up session. Distributions were computed by generating 10,000 bootstrapped randomly sampled observations and fitting the model for each sample. Distributions outlined in red delineate distributions that are significantly different from zero (α = 0.05, non-parametric 95% CI, 10,000 bootstraps) (EPS 12938 kb)
11682_2018_9983_MOESM2_ESM.eps (13 mb)
Fig. S2 Distributions of estimated \( {\widehat{R^2}}_{Th,j} \) value at each follow-up session. Distributions were computed by generating 10,000bootstrapped randomly sampled observations and fitting the model for each sample. Distributions outlined in red delineate distributions that are significantly different from zero (α = 0.05, non-parametric 95% CI, 10,000 bootstraps) (EPS 13264 kb)

References

  1. 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
  2. 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
  3. 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
  4. Bailes, J. E., Petraglia, A. L., Omalu, B. I., Nauman, E., & Talavage, T. (2013). Role of subconcussion in repetitive mild traumatic brain injury. Journal of Neurosurgery, 119(5), 1235–1245.  https://doi.org/10.3171/2013.7.JNS121822.CrossRefPubMedGoogle Scholar
  5. 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.
  6. Barkhoudarian, G., Hovda, D. A., & Giza, C. C. (2011). The molecular pathophysiology of concussive brain injury. Clinical Sports Medicine, 30(1), 33–48.CrossRefGoogle Scholar
  7. 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
  8. 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
  9. Becelewski, J., & Pierzchala, K. (2003). Cerebrovascular reactivity in patients with mild head injury. Neurologia i Neurochirurgia Polska, 37(2), 339–350.PubMedGoogle Scholar
  10. 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
  11. Bright, M. G., & Murphy, K. (2013). Reliable quantification of BOLD fMRI cerebrovascular reactivity despite poor breath-hold performance. Neuroimage, 83, 559–568.  https://doi.org/10.1016/j.neuroimage.2013.07.007.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Broshek, D. K., Kaushik, T., Freeman, J. R., Erlanger, D., Webbe, F., & Barth, J. T. (2005). Sex differences in outcome following sports-related concussion. Journal of Neurosurgery, 102(5), 856–863.CrossRefGoogle Scholar
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. Delaney, J. S., Lacroix, V. J., Leclerc, S., & Jonston, K. (2002). Concussions Among University Football and Soccer Players. Clinical Journal of Sport Medicine, 12, 331–338.CrossRefGoogle Scholar
  19. Duhaime, A. C., Gennarelli, T. A., Thibault, L. E., Bruce, D. A., Margulies, S. S., & Wiser, R. (1987). The shaken baby syndrome. A clinical, pathological, and biomechanical study. Journal of Neurosurgery, 66(3), 409–415.  https://doi.org/10.3171/jns.1987.66.3.0409.CrossRefPubMedGoogle Scholar
  20. 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
  21. Giza, C. C., & Hovda, D. A. (2001). The Neurometabolic Cascade of Concussion. Journal of Athletic Training, 36(3), 228–235.PubMedPubMedCentralGoogle Scholar
  22. Golding, E. M., Robertson, C. S., & Bryan Jr., R. M. (1999). The consequences of traumatic brain injury on cerebral blood flow and autoregulation: a review. Clinical and Experimental Hypertension, 21(4), 299–332.CrossRefGoogle Scholar
  23. 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
  24. Kastrup, A., Gunnar, K., Neumann-Haefelin, T., & Moseley, M. (2001). Assessment of cerebrovascular reactivity with functional magnetic resonance imaging: comparison of C02 and Breath Holding. Magnetic Resonance Imaging, 19, 13–20.CrossRefGoogle Scholar
  25. Koerte, I. K., Lin, A. P., Willems, A., Muehlmann, M., Hufschmidt, J., Coleman, M. J., et al. (2015). A review of neuroimaging findings in repetitive brain trauma. Brain Pathology, 25(3), 318–349.  https://doi.org/10.1111/bpa.12249.CrossRefPubMedGoogle Scholar
  26. Len, T. K., & Neary, J. P. (2011). Cerebrovascular pathophysiology following mild traumatic brain injury. Clinical Physiology and Functional Imaging, 31(2), 85–93.  https://doi.org/10.1111/j.1475-097X.2010.00990.x.CrossRefPubMedGoogle Scholar
  27. 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
  28. 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
  29. Lipp, I., Murphy, K., Caseras, X., & Wise, R. G. (2015). Agreement and repeatability of vascular reactivity estimates based on a breath-hold task and a resting state scan. Neuroimage, 113, 387–396.  https://doi.org/10.1016/j.neuroimage.2015.03.004.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lipton, M. L., Kim, N., Zimmerman, M. E., Kim, M., Stewart, W. F., Branch, C. A., et al. (2013). Soccer Heading is Assciated with White Matter Microstructural and Cognitive Abnormalities. Radiology, 268(3), 850–857.CrossRefGoogle Scholar
  31. Marar, M., McIlvain, N. M., Fields, S. K., & Comstock, R. D. (2012). Epidemiology of concussions among United States high school athletes in 20 sports. The American Journal of Sports Medicine, 40(4), 747–755.  https://doi.org/10.1177/0363546511435626.CrossRefPubMedGoogle Scholar
  32. Maugans, T. A., Farley, C., Altaye, M., Leach, J., & Cecil, K. M. (2012). Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics, 129(1), 28–37.  https://doi.org/10.1542/peds.2011-2083.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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
  34. McCuen, E. C., Svaldi, D. O., Breedlove Morigaki, K., Kraz, N., Cummiskey, B., Breedlove, E., et al. (2015). Colleigate Women's Soccer Players Suffer Greater Cumulative Head Impacts than their High School Counterparts. Journal of Biomechanics, 48(13), 3720–3723.CrossRefGoogle Scholar
  35. Meaney, D. F., & Smith, D. H. (2011). Biomechanics of concussion. Clinics in Sports Medicine, 30(1), 19–31, vii.  https://doi.org/10.1016/j.csm.2010.08.009.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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
  37. 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/.
  38. Mutch, W. A., Ellis, M. J., Graham, M. R., Wourms, V., Raban, R., Fisher, J. A., et al. (2014). Brain MRI CO2 stress testing: a pilot study in patients with concussion. PLoS One, 9(7), e102181.  https://doi.org/10.1371/journal.pone.0102181.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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
  40. Ommaya, A. K., Faas, F., & Yarnell, P. (1968). Whiplash injury and brain damage: an experimental study. JAMA, 204(4), 285–289.CrossRefGoogle Scholar
  41. Peirce, J. W. (2007). PsychoPy--Psychophysics software in Python. Journal of Neuroscience Methods, 162(1–2), 8–13.  https://doi.org/10.1016/j.jneumeth.2006.11.017.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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
  43. 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
  44. 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
  45. 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
  46. Shenk, T. E., Robinson, M. E., Svaldi, D. O., Abbas, K., Breedlove, K. M., Leverenz, L. J., et al. (2015). FMRI of visual working memory in high school football players. Developmental Neuropsychology, 40(2), 63–68.  https://doi.org/10.1080/87565641.2015.1014088.CrossRefPubMedGoogle Scholar
  47. 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
  48. 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
  49. Stein, T. D., Alvarez, V. E., & McKee, A. C. (2015). Concussion in Chronic Traumatic Encephalopathy. Current Pain and Headache Reports, 19(10), 47.  https://doi.org/10.1007/s11916-015-0522-z.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Stewart, W. F., Kim, N., Ifrah, C., Bachrach, T. A., Zimmerman, M. E., Kim, M., et al. (2017). Symptoms from repeated intentional and unintentional head impact in soccer players. Neurology, 88, 901–908.CrossRefGoogle Scholar
  51. 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
  52. 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
  53. 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
  54. 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
  55. Talavage, T. M., Nauman, E. A., & Leverenz, L. J. (2015). The Role of Medical Imaging in the Recharacterization of Mild Traumatic Brain Injury Using Youth Sports as a Laboratory. [Review]. Frontiers in Neurology, 6, 273.  https://doi.org/10.3389/fneur.2015.00273.CrossRefPubMedGoogle Scholar
  56. Wang, Y., Nelson, L. D., LaRoche, A. A., Pfaller, A. Y., Nencka, A. S., Koch, K. M., et al. (2016). Cerebral Blood Flow Alterations in Acute Sport-Related Concussion. Journal of Neurotrauma, 33(13), 1227–1236.  https://doi.org/10.1089/neu.2015.4072.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Weldon School of Biomedical EngineeringPurdue UniversityWest LafayetteUSA
  2. 2.Department of NeurologyIndiana University School of MedicineIndianapolisUSA
  3. 3.School of Electrical and Computer EngineeringPurdue UniversityWest LafayetteUSA
  4. 4.School of Mechanical EngineeringPurdue UniversityWest LafayetteUSA
  5. 5.School of Chemical EngineeringPurdue UniversityWest LafayetteUSA
  6. 6.Department of Child PsychologyPurdue UniversityWest LafayetteUSA
  7. 7.Department of PediatricsIndiana University School of MedicineIndianapolisUSA
  8. 8.Department of Health and KinesiologyPurdue UniversityWest LafayetteUSA

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