Skip to main content
SpringerLink
Log in

Cerebrovascular reactivity changes in asymptomatic female athletes attributable to high school soccer participation

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. doi:10.3171/2013.7.jns121822.

    Article  PubMed  Google 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 

  • Bazarian, J. J., Zhu, T., Blyth, B., Borrino, A., & Zhong, J. (2012). Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magnetic Resonance Imaging, 30(2), 171–180. doi:10.1016/j.mri.2011.10.001.

    Article  PubMed  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 

  • Birn, R. M., Smith, M. A., Jones, T. B., & Bandettini, P. A. (2008). The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. NeuroImage, 40(2), 644–654. doi:10.1016/j.neuroimage.2007.11.059.

    Article  PubMed  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.

    Article  Google Scholar 

  • Bright, M. G., Bulte, D. P., Jezzard, P., & Duyn, J. H. (2009). Characterization of regional heterogeneity in cerebrovascular reactivity dynamics using novel hypocapnia task and BOLD fMRI. NeuroImage, 48(1), 166–175. doi:10.1016/j.neuroimage.2009.05.026.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bright, M. G., & Murphy, K. (2013). Reliable quantification of BOLD fMRI cerebrovascular reactivity despite poor breath-hold performance. NeuroImage, 83, 559–568. doi:10.1016/j.neuroimage.2013.07.007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Broglio, S. P., Eckner, J. T., Martini, D., Sosnoff, J. J., Kutcher, J. S., & Randolph, C. (2011). Cumulative head impact burden in high school football. Journal of Neurotrauma, 28(10), 2069–2078. doi:10.1089/neu.2011.1825.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google Scholar 

  • Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.

    Article  CAS  PubMed  Google Scholar 

  • De Kruijk, J. R., Twijnstra, A., & Leffers, P. (2001). Diagnostic criteria and differential diagnosis of mild traumatic brain injury. Brain Injury, 15(2), 99–106. doi:10.1080/026990501458335.

    Article  PubMed  Google Scholar 

  • Delaney, J. S., Lacroix, V. J., Leclerc, S., & Jonston, K. (2002). Concussions among university football and soccer players. Clinical Journal of Sports Medicine, 12, 331–338.

    Article  Google 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.

    Article  PubMed  Google Scholar 

  • Fuller, C. W., Junge, A., & Dvorak, J. (2005). A six year prospective study of the incidence and causes of head and neck injuries in international football. British Journal of Sports Medicine, 39(Suppl 1), i3–i9. doi:10.1136/bjsm.2005.018937.

    Article  PubMed  PubMed Central  Google 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.

    Article  PubMed  Google Scholar 

  • Gessel, L. M., Fields, S. K., Collins, C. L., Dick, R. W., & Comstock, R. D. (2007). Concussions among United States high school and collegiate athletes. Journal of Athletic Training, 42(4), 495–503.

    PubMed  PubMed Central  Google Scholar 

  • Giza, C. C., & Hovda, D. A. (2001). The Neurometabolic Cascade of Concussion. Journal of Athletic Training, 36(3), 228–235 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12937489.

    PubMed  PubMed Central  Google 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.

    CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google Scholar 

  • Jordan, B. D., & Bailes, J. (2000). Concussion history and current neurological symptoms among retired professional football players. Neurology, 54, A410–A411.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Len, T. K., & Neary, J. P. (2011). Cerebrovascular pathophysiology following mild traumatic brain injury. Clinical Physiology and Functional Imaging, 31(2), 85–93. doi:10.1111/j.1475-097X.2010.00990.x.

    CAS  PubMed  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.

    Article  PubMed  Google 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 

  • 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. doi:10.1016/j.neuroimage.2015.03.004.

    Article  PubMed  PubMed Central  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).

  • 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. doi:10.1177/0363546511435626.

    Article  PubMed  Google Scholar 

  • Marchi, N., Bazarian, J. J., Puvenna, V., Janigro, M., Ghosh, C., Zhong, J., et al. (2013). Consequences of repeated blood-brain barrier disruption in football players. PloS One, 8(3), e56805. doi:10.1371/journal.pone.0056805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. doi:10.1542/peds.2011-2083.

    Article  PubMed  PubMed Central  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.

    Article  PubMed  PubMed Central  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

  • 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.

    Article  PubMed  Google 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/

  • Murphy, K., Harris, A. D., & Wise, R. G. (2011). Robustly measuring vascular reactivity differences with breath-hold: normalising stimulus-evoked and resting state BOLD fMRI data. NeuroImage, 54(1), 369–379. doi:10.1016/j.neuroimage.2010.07.059.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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. doi:10.1371/journal.pone.0102181.

    Article  PubMed  PubMed Central  Google Scholar 

  • Peirce, J. W. (2007). PsychoPy–psychophysics software in python. Journal of Neuroscience Methods, 162(1–2), 8–13. doi:10.1016/j.jneumeth.2006.11.017.

    Article  PubMed  PubMed Central  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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. doi:10.1080/87565641.2015.1012204.

    Article  PubMed  Google Scholar 

  • Rosenthal, J. A., Foraker, R. E., Collins, C. L., & Comstock, R. D. (2014). National high school athlete concussion rates from 2005 to 2006 to 2011–2012. The American Journal of Sports Medicine, 42(7), 1710–1715. doi:10.1177/0363546514530091.

    Article  PubMed  Google 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.

    Article  CAS  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google Scholar 

  • 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. doi:10.1080/87565641.2015.1014088.

    Article  PubMed  Google Scholar 

  • Sim, A., Terryberry-Spohr, L., & Wilson, K. R. (2008). Prolonged recovery of memory functioning after mild traumatic brain injury in adolescent athletes. Journal of Neurosurgery, 108(3), 511–516. doi:10.3171/JNS/2008/108/3/0511.

    Article  PubMed  Google Scholar 

  • Slobounov, S., Sebastianelli, W., & Hallett, M. (2012). Residual brain dysfunction observed one year post-mild traumatic brain injury: combined EEG and balance study. Clinical Neurophysiology, 123(9), 1755–1761. doi:10.1016/j.clinph.2011.12.022.

    Article  PubMed  PubMed Central  Google Scholar 

  • Snowden, J. S., Neary, D., & Mann, D. M. (2002). Frontotemporal dementia. The British Journal of Psychiatry, 180, 140–143 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11823324.

    Article  PubMed  Google 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. doi:10.1080/87565641.2014.973959.

    Article  PubMed  Google 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.

    Article  PubMed  PubMed Central  Google 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yezhuvath, U. S., Uh, J., Cheng, Y., Martin-Cook, K., Weiner, M., Diaz-Arrastia, R., et al. (2012). Forebrain-dominant deficit in cerebrovascular reactivity in Alzheimer's disease. Neurobiology of Aging, 33(1), 75–82. doi:10.1016/j.neurobiolaging.2010.02.005.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google 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 

Download references

Author information

Authors and Affiliations

  1. Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, 4907, USA

    Diana O. Svaldi, Emily C. McCuen, Robert Hannemann, Eric A. Nauman & Thomas M. Talavage

  2. School of Electrical and Computer Engineering, Purdue University, West Lafayette, IN, 47907, USA

    Chetas Joshi & Thomas M. Talavage

  3. School of Chemical Engineering, Purdue University, West Lafayette, IN, 47907, USA

    Meghan E. Robinson

  4. Department of Psychology, University of California, Berkeley, CA, 94729, USA

    Yeseul Nho

  5. Neuroimaging Research for Veterans (NeRVe) Center, VA Boston Healthcare System, Boston, MA, 02130, USA

    Robert Hannemann

  6. School of Mechanical Engineering, Purdue University, West Lafayette, IN, 47907, USA

    Eric A. Nauman

  7. Department of Health and Kinesiology, Purdue University, West Lafayette, IN, 47907, USA

    Larry J. Leverenz

  8. Concussion Neuroimaging Consortium, Purdue University, West Lafayette, IN, 47907, USA

    Eric A. Nauman, Larry J. Leverenz & Thomas M. Talavage

Authors
  1. Diana O. Svaldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emily C. McCuen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chetas Joshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meghan E. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yeseul Nho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert Hannemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eric A. Nauman
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Larry J. Leverenz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Thomas M. Talavage
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diana O. Svaldi.

Ethics declarations

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.

Funding

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 consent

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.

Electronic supplementary material

ESM 1

(DOCX 23.5 kb)

ESM 2

(DOCX 23.6 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Svaldi, D.O., McCuen, E.C., Joshi, C. et al. Cerebrovascular reactivity changes in asymptomatic female athletes attributable to high school soccer participation. Brain Imaging and Behavior 11, 98–112 (2017). https://doi.org/10.1007/s11682-016-9509-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-016-9509-6

Keywords

Search

Navigation