Cerebrovascular reactivity changes in asymptomatic female athletes attributable to high school soccer participation
As participation in women’s soccer continues to grow and the longevity of female athletes’ careers continues to increase, prevention and care for mTBI in women’s soccer has become a major concern for female athletes since the long-term risks associated with a history of mTBI are well documented. Among women’s sports, soccer exhibits among the highest concussion rates, on par with those of men’s football at the collegiate level. Head impact monitoring technology has revealed that “concussive hits” occurring directly before symptomatic injury are not predictive of mTBI, suggesting that the cumulative effect of repetitive head impacts experienced by collision sport athletes should be assessed. Neuroimaging biomarkers have proven to be valuable in detecting brain changes that occur before neurocognitive symptoms in collision sport athletes. Quantifying the relationship between changes in these biomarkers and head impacts experienced by female soccer athletes may prove valuable to developing preventative measures for mTBI. This study paired functional magnetic resonance imaging with head impact monitoring to track cerebrovascular reactivity changes throughout a season and to test whether the observed changes could be attributed to mechanical loading experienced by female athletes participating in high school soccer. Marked cerebrovascular reactivity changes were observed in female soccer athletes, relative both to non-collision sport control measures and pre-season measures and were localized to fronto-temporal aspects of the brain. These changes persisted 4–5 months after the season ended and recovered by 8 months after the season. Segregation of the total soccer cohort into cumulative loading groups revealed that population-level changes were driven by athletes experiencing high cumulative loads, although athletes experiencing lower cumulative loads still contributed to group changes. The results of this study imply a non-linear relationship between cumulative loading and cerebrovascular changes with a threshold, above which the risk, of injury likely increases significantly.
KeywordsMild traumatic brain injury Collision sports Head impacts Cerebrovascular reactivity Soccer
Compliance with ethical standards
All procedures performed in studies involving human participants were approved by the Purdue IRB and 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.
This study was funded by BrainScope Company, Inc., and General Electric Healthcare.
Conflict of interest
Author Diana Otero Svaldi declares that she has no conflict of interest. Author Emily McCuen declares that she has no conflict of interest. Author Chetas Joshi declares that he has no conflict of interest. Author Yeseul Nho declares that she has no conflict of interest. Author Meghan Robinson declares that she has no conflict of interest. Author Robert Hanneman declares that he has no conflict of interest. Author Larry Leverenz declares that he has no conflict of interest. Author Eric Nauman declares that he has no conflict of interest. Author Thomas Talavage declares that he has no conflict of interest.
Informed parent consent and subject assent was obtained for all subjects under the age of 18. Informed consent was obtained for all subjects 18 or older.
- Abbas, K., Shenk, T. E., Poole, V. N., Robinson, M. E., Leverenz, L. J., Nauman, E. A., & Talavage, T. M. (2015). Effects of repetitive sub-concussive brain injury on the functional connectivity of default mode network in high school football athletes. Developmental Neuropsychology, 40(1), 51–56. doi: 10.1080/87565641.2014.990455.CrossRefPubMedGoogle Scholar
- Ainslie, P. N., Cotter, J. D., George, K. P., Lucas, S., Murrell, C., Shave, R., & Atkinson, G. (2008). Elevation in cerebral blood flow velocity with aerobic fitness throughout healthy human ageing. The Journal of Physiology, 586(16), 4005–4010. doi: 10.1113/jphysiol.2008.158279.CrossRefPubMedPubMedCentralGoogle Scholar
- Barth, J. T., Freeman, J. R., Broshek, D. K., & Varney, R. N. (2001). Acceleration-Deceleration Sport-Related Concussion: The Gravity of It All. Journal of Athletic Train, 36(3), 253–256 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12937493 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC155415/pdf/attr_36_03_0253.pdf.Google Scholar
- Becelewski, J., & Perzchala, K. (2003). Cerebrovascular reactivity in patients with mild head injury. Polish Journal of Neurology and Neurosurgery, 37(2), 339–350.Google Scholar
- Breedlove, K. M., Breedlove, E. L., Robinson, M., Poole, V. N., King, J. R. I., Rosenberger, P., et al. (2014). Detecting neurocognitive & neurophysiological changes as a result of subconcussive blows in high school football athletes. Athletic Training and Sports Healthcare, 6(3), 119–127.CrossRefGoogle 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. doi: 10.3109/02699052.2014.974209.CrossRefPubMedGoogle Scholar
- Desikan, R. S., Segonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980. doi: 10.1016/j.neuroimage.2006.01.021.CrossRefPubMedGoogle Scholar
- Gao, Y., Zhang, J., Liu, H., Wu, G., Xiong, L., & Shu, M. (2013). Regional cerebral blood flow and cerebrovascular reacvitity in Alzheimer’s disease and vascular dementia assessed by arterial spin labeling magnetic resonance imaging. Current Neurovascular Research, 10, 49–53.CrossRefPubMedGoogle Scholar
- Golding, E. M., Steenberg, M. L., Contant Jr., C. F., Krishnappa, I., Robertson, C. S., & Bryan Jr., R. M. (1999). Cerebrovascular reactivity to CO(2) and hypotension after mild cortical impact injury. American Journal of Physiology, 277(4 Pt 2), H1457–H1466 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10516183.PubMedGoogle Scholar
- Guskiewicz, K. M., Marshall, S. W., Bailes, J., McCrea, M., Cantu, R. C., Randolph, C., & Jordan, B. D. (2005). Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery, 719–726. doi: 10.1227/01.neu.0000175725.75780.dd.
- Guskiewicz, K. M., Marshall, S. W., Bailes, J., McCrea, M., Harding Jr., H. P., Matthews, A., et al. (2007a). Recurrent concussion and risk of depression in retired professional football players. Medicine and Science in Sports and Exercise, 39(6), 903–909. doi: 10.1249/mss.0b013e3180383da5.CrossRefPubMedGoogle Scholar
- Guskiewicz, K. M., McCrea, M., Marshall, S. W., Cantu, R. C., Randolph, C., Barr, W., et al. (2003). Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA concussion study. Jama, 290(19), 2549–2555. doi: 10.1001/jama.290.19.2549.CrossRefPubMedGoogle Scholar
- Guskiewicz, K. M., Mihalik, J. P., Shankar, V., Marshall, S. W., Crowell, D. H., Oliaro, S. M., et al. (2007b). Measurement of head impacts in collegiate football players: relationship between head impact biomechanics and acute clinical outcome after concussion. Neurosurgery, 61(6), 1244–1252 discussion 1252-1243. doi: 10.1227/01.neu.0000306103.68635.1a.CrossRefPubMedGoogle Scholar
- Jordan, B. D., & Bailes, J. (2000). Concussion history and current neurological symptoms among retired professional football players. Neurology, 54, A410–A411.Google Scholar
- Len, T. K., Neary, J. P., Asmundson, G. J., Candow, D. G., Goodman, D. G., Bjornson, B., & Bhambhani, Y. N. (2013). Serial monitoring of CO2 reactivity following sport concussion using hypocapnia and hypercapnia. Brain Injury, 27(3), 346–353. doi: 10.3109/02699052.2012.743185.CrossRefPubMedGoogle Scholar
- Lewis, P. M., Czosnyka, M., Smielewski, P., & J.D., P. (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
- Lovell, M., Collins, M. W., Iverson, G. L., Field, M., Maroon, J. C., Cantu, R., et al. (2003). Recovery from mild concussion in high school athletes. Neurosurgery, 98(295–301).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. doi: 10.1212/01.wnl.0000438220.16190.42.CrossRefPubMedPubMedCentralGoogle Scholar
- McAllister, T. W., Saykin, A. J., Flashman, L. A., Sparling, M. B., Johnson, S. C., Guerin, S. J., et al. (1999). Brain activation during working memory 1 month after mild traumatic brain injury: a functional MRI study. Neurology, 53(6), 1300–1308 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10522888.CrossRefPubMedGoogle Scholar
- McCaffrey, M. A., Mihalik, J. P., Crowell, D. H., Shields, E. W., & Guskiewicz, K. M. (2007). Measurement of head impacts in collegiate football players: clinical measures of concussion after high- and low-magnitude impacts. Neurosurgery, 61(6), 1236–1243 discussion 1243. doi: 10.1227/01.neu.0000306102.91506.8b.CrossRefPubMedGoogle Scholar
- McCuen, E. C., Svaldi, D. O., Breedlove Morigaki, K., Kraz, N., Cummiskey, B., Breedlove, E.,... Nauman, E. A. (2015). Colleigate women's soccer players suffer greater cumulative head impacts than their high school counterparts Journal of Biomechanics.Google Scholar
- Mihalik, J. P., Bell, D. R., Marshall, S. W., & Guskiewicz, K. M. (2007). Measurement of head impacts in collegiate football players: an investigation of positional and event-type differences. Neurosurgery, 61(6), 1229–1235 discussion 1235. doi: 10.1227/01.neu.0000306101.83882.c8.CrossRefPubMedGoogle Scholar
- Militana, A. R., Donahue, M. J., Sills, A. K., Solomon, G. S., Gregory, A. J., Strother, M. K., & Morgan, V. L. (2015). Alterations in default-mode network connectivity may be influenced by cerebrovascular changes within 1 week of sports related concussion in college varsity athletes: a pilot study. Brain Imaging and Behavior. doi: 10.1007/s11682-015-9407-3.Google Scholar
- Morris, B. (2015). Why Is the U.S. So Good at Women's Soccer? Retrieved from http://fivethirtyeight.com/datalab/why-is-the-u-s-so-good-at-womens-soccer/
- Murrell, C. J., Cotter, J. D., Thomas, K. N., Lucas, S. J., Williams, M. J., & Ainslie, P. N. (2013). Cerebral blood flow and cerebrovascular reactivity at rest and during sub-maximal exercise: effect of age and 12-week exercise training. Age (Dordrecht, Netherlands), 35(3), 905–920. doi: 10.1007/s11357-012-9414-x.CrossRefGoogle 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. doi: 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). Sub-concussive hit characteristics predict deviant brain metabolism in football athletes. Developmental Neuropsychology, 40(1), 12–17. doi: 10.1080/87565641.2014.984810.CrossRefPubMedGoogle Scholar
- Rosso, S. M., Landweer, E. J., Houterman, M., Donker Kaat, L., van Duijn, C. M., & van Swieten, J. C. (2003). Medical and environmental risk factors for sporadic frontotemporal dementia: a retrospective case-control study. Journal of Neurology, Neurosurgery & Psychiatry, 74(11), 1574–1576 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/14617722.CrossRefGoogle Scholar
- Schnebel, B., Gwin, J. T., Anderson, S., & Gatlin, R. (2007). In vivo study of head impacts in football: a comparison of national collegiate athletic association division I versus high school impacts. Neurosurgery, 60(3), 490–495 discussion 495-496. doi: 10.1227/01.NEU.0000249286.92255.7F.CrossRefPubMedGoogle Scholar
- Schulz, M. R., Marshall, S. W., Mueller, F. O., Yang, J., Weaver, N. L., Kalsbeek, W. D., & Bowling, J. M. (2004). Incidence and risk factors for concussion in high school athletes, North Carolina, 1996–1999. American Journal of Epidemiology, 160(10), 937–944. doi: 10.1093/aje/kwh304.CrossRefPubMedGoogle 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. doi: 10.1089/neu.2010.1512.CrossRefPubMedPubMedCentralGoogle Scholar
- Wang, Y., West, J. D., Bailey, J. N., Westfall, D. R., Xiao, H., Arnold, T. W., et al. (2015). Decreased cerebral blood flow in chronic pediatric mild TBI: an MRI perfusion study. Developmental Neuropsychology, 40(1), 40–44. doi: 10.1080/87565641.2014.979927.CrossRefPubMedPubMedCentralGoogle Scholar
- Zhang, F., Sprague, S. M., Farrokhi, F., Henry, M. N., Son, M. G., & Vollmer, D. G. (2002). Reversal of attenuation of cerebrovascular reactivity to hypercapnia by a nitric oxide donor after controlled cortical impact in a rat model of traumatic brain injury. Journal of Neurosurgery, 97(4), 963–969. doi: 10.3171/jns.2002.97.4.0963.CrossRefPubMedGoogle Scholar
- Zuckerman, S. L., Kerr, Z. Y., Yengo-Kahn, A., Wasserman, E., Covassin, T., & Solomon, G. S. (2015). Epidemiology of sports-related concussion in NCAA athletes from 2009 to 2010 to 2013–2014: incidence, recurrence, and mechanisms. The American Journal of Sports Medicine. doi: 10.1177/0363546515599634.Google Scholar