Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-21T13:53:31.629Z Has data issue: false hasContentIssue false
  • English
  • Français

The Effect of Aerobic Exercise on Concussion Recovery: A Pilot Clinical Trial

Published online by Cambridge University Press:  16 November 2021

Aliyah R. Snyder Open the ORCID record for Aliyah R. Snyder [Opens in a new window] ,
Sarah M. Greif ,
James R. Clugston ,
David B. FitzGerald ,
Joshua F. Yarrow ,
Talin Babikian ,
Christopher C. Giza ,
Floyd J. Thompson  and
Russell M. Bauer
Aliyah R. Snyder*
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, USA UCLA Steve Tisch BrainSPORT Program, University of California, Los Angeles, Los Angeles, CA, USA
Sarah M. Greif
Affiliation:
Department of Clinical and Health Psychology, University of Florida, Gainesville, FL, USA Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, CA, USA
James R. Clugston
Affiliation:
Department of Community Health and Family Medicine, University of Florida, Gainesville, FL, USA
David B. FitzGerald
Affiliation:
Department of Neurology, University of Florida, Gainesville, FL, USA Research Service and Brain Rehabilitation Research Center, Malcolm Randall VA Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA
Joshua F. Yarrow
Affiliation:
Research Service and Brain Rehabilitation Research Center, Malcolm Randall VA Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA Division of Endocrinology, Diabetes, and Metabolism, University of Florida College of Medicine, Gainesville, FL, USA
Talin Babikian
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, USA UCLA Steve Tisch BrainSPORT Program, University of California, Los Angeles, Los Angeles, CA, USA Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, CA, USA
Christopher C. Giza
Affiliation:
UCLA Steve Tisch BrainSPORT Program, University of California, Los Angeles, Los Angeles, CA, USA Mattel Children’s Hospital, University of California, Los Angeles, Los Angeles, CA, USA Department of Pediatrics, University of California, Los Angeles, Los Angeles, CA, USA
Floyd J. Thompson
Affiliation:
Research Service and Brain Rehabilitation Research Center, Malcolm Randall VA Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA Department of Physiological Sciences, University of Florida, Gainesville, FL, USA Department of Neuroscience, University of Florida, Gainesville, FL, USA
Russell M. Bauer
Affiliation:
Department of Clinical and Health Psychology, University of Florida, Gainesville, FL, USA Research Service and Brain Rehabilitation Research Center, Malcolm Randall VA Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA
*
*Correspondence and reprint requests to: Aliyah R. Snyder, University of California, Los Angeles, 760 Westwood Plaza, Room 18-240, Los Angeles, CA, 90095, USA. Email: asnyder@mednet.ucla.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

The purpose of this study was to pilot safety and tolerability of a 1-week aerobic exercise program during the post-acute phase of concussion (14–25 days post-injury) by examining adherence, symptom response, and key functional outcomes (e.g., cognition, mood, sleep, postural stability, and neurocognitive performance) in young adults.

Method:

A randomized, non-blinded pilot clinical trial was performed to compare the effects of aerobic versus non-aerobic exercise (placebo) in concussion patients. The study enrolled three groups: 1) patients with concussion/mild traumatic brain injury (mTBI) randomized to an aerobic exercise intervention performed daily for 1-week, 2) patients with concussion/mTBI randomized to a non-aerobic (stretching and calisthenics) exercise program performed daily for 1-week, and 3) non-injured, no intervention reference group.

Results:

Mixed-model analysis of variance results indicated a significant decrease in symptom severity scores from pre- to post-intervention (mean difference = −7.44, 95% CI [−12.37, −2.20]) for both concussion groups. However, the pre- to post-change was not different between groups. Secondary outcomes all showed improvements by post-intervention, but no differences in trajectory between the groups. By three months post-injury, all outcomes in the concussion groups were within ranges of the non-injured reference group.

Conclusions:

Results from this study indicate that the feasibility and tolerability of administering aerobic exercise via stationary cycling in the post-acute time frame following post-concussion (14–25 days) period are tentatively favorable. Aerobic exercise does not appear to negatively impact recovery trajectories of neurobehavioral outcomes; however, tolerability may be poorer for patients with high symptom burden.

Keywords

NeuropsychologyReturn to SportBrain InjuriesSportsFeasibility StudiesPublic Health
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 27 , Issue 8 , September 2021 , pp. 790 - 804
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albanes, D., Conway, J.M., Taylor, P.R., Moe, P.W., & Judd, J. (1990). Validation and comparison of eight physical activity questionnaires. Epidemiology. https://doi.org/10.1097/00001648-199001000-00014 Google ScholarPubMed
Allen, R.P., Kosinski, M., Hill-Zabala, C.E., & Calloway, M.O. (2009). Psychometric evaluation and tests of validity of the Medical Outcomes Study 12-item Sleep Scale (MOS sleep). Sleep Medicine. 10(5), 531–539. https://doi.org/10.1016/j.sleep.2008.06.003 CrossRefGoogle Scholar
Asken, B.M., Bauer, R.M., Guskiewicz, K.M., McCrea, M.A., Schmidt, J.D., Giza, C.C., … Svoboda, S. (2018). Immediate removal from activity after sport-related concussion is associated with shorter clinical recovery and less severe symptoms in collegiate student-athletes. American Journal of Sports Medicine, 46(6), 1465–1474. https://doi.org/10.1177/0363546518757984 Google ScholarPubMed
Asken, B.M., McCrea, M.A., Clugston, J.R., Snyder, A.R., Houck, Z.M., & Bauer, R.M. (2016). Playing through it: Delayed reporting and removal from athletic activity after concussion predicts prolonged recovery. Journal of Athletic Training, 51(4), 329–335. https://doi.org/10.4085/1062-6050-51.5.02 CrossRefGoogle ScholarPubMed
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
Beglinger, L.J., Gaydos, B., Tangphao-Daniels, O., Duff, K., Kareken, D.A., Crawford, J., … Siemers, E.R. (2005). Practice effects and the use of alternate forms in serial neuropsychological testing. Archives of Clinical Neuropsychology, 20(4), 517–529. https://doi.org/10.1016/j.acn.2004.12.003 CrossRefGoogle ScholarPubMed
Benton, A.L. (1969). Development of a multilingual aphasia battery. Progress and problems. Journal of the Neurological Sciences, 9(1), 39–48. https://doi.org/10.1016/0022-510X(69)90057-4 Google ScholarPubMed
Bigler, E.D. (2007). Neuropsychology and clinical neuroscience of persistent post-concussive syndrome. Journal of the International Neuropsychological Society, 14(1), 1–22. https://doi.org/10.1017/S135561770808017X CrossRefGoogle Scholar
Boisgontier, M.P. & Cheval, B. (2016). The anova to mixed model transition. Neuroscience & Biobehavioral Reviews, 68, 1004–1005. https://doi.org/10.1016/j.neubiorev.2016.05.034 CrossRefGoogle ScholarPubMed
Borg, J., Holm, L., Peloso, P.M., Cassidy, J.D., Carroll, L.J., von Holst, H., … Yates, D. (2004). Non-surgical intervention and cost for mild traumatic brain injury: Results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. Journal of Rehabilitation Medicine, (43 Suppl.). https://doi.org/10.1080/16501960410023840 Google ScholarPubMed
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). https://doi.org/10.3171/jns.2005.102.5.0856 CrossRefGoogle ScholarPubMed
Brown, D.A., Elsass, J.A., Miller, A.J., Reed, L.E., & Reneker, J.C. (2015). Differences in symptom reporting between males and females at baseline and after a sports-related concussion: A systematic review and meta-analysis. Sports Medicine, 45(7), 1027–1040. https://doi.org/10.1007/s40279-015-0335-6 CrossRefGoogle ScholarPubMed
Calamia, M., Markon, K., & Tranel, D. (2012). Scoring higher the second time around: Meta-analyses of practice effects in neuropsychological assessment. Clinical Neuropsychologist, 26(4), 543–570. https://doi.org/10.1080/13854046.2012.680913 CrossRefGoogle ScholarPubMed
Chan, J.S.Y., Liu, G., Liang, D., Deng, K., Wu, J., & Yan, J.H. (2019). Special issue–therapeutic benefits of physical activity for mood: A systematic review on the effects of exercise intensity, duration, and modality. Journal of Psychology: Interdisciplinary and Applied, 153(1), 102–125. https://doi.org/10.1080/00223980.2018.1470487 CrossRefGoogle ScholarPubMed
Charek, D.B., Elbin, R.J., Sufrinko, A., Schatz, P., D’Amico, N.R., Collins, M.W., & Kontos, A.P. (2019). Preliminary evidence of a dose-response for continuing to play on recovery time after concussion. Journal of Head Trauma Rehabilitation, 35(2), 85–91. https://doi.org/10.1097/HTR.0000000000000476 CrossRefGoogle Scholar
Chennaoui, M., Arnal, P.J., Sauvet, F., & Léger, D. (2015). Sleep and exercise: A reciprocal issue? Sleep Medicine Reviews, 20, 59–72. https://doi.org/10.1016/j.smrv.2014.06.008 Google ScholarPubMed
Chin, E.Y., Nelson, L.D., Barr, W.B., McCrory, P., & McCrea, M.A. (2016). Reliability and validity of the sport concussion assessment tool-3 (SCAT3) in high school and collegiate athletes. American Journal of Sports Medicine, 44(9), 2276–2285. https://doi.org/10.1177/0363546516648141 CrossRefGoogle ScholarPubMed
Coelho, F.G. de M., Gobbi, S., Andreatto, C.A.A., Corazza, D.I., Pedroso, R.V., & Santos-Galduróz, R.F. (2013). Physical exercise modulates peripheral levels of brain-derived neurotrophic factor (BDNF): A systematic review of experimental studies in the elderly. Archives of Gerontology and Geriatrics, 56(1), 10–15. https://doi.org/10.1016/j.archger.2012.06.003 CrossRefGoogle ScholarPubMed
Covassin, T., Elbin, R.J., Harris, W., Parker, T., & Kontos, A. (2012). The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. American Journal of Sports Medicine, 40(6), 1303–1312. https://doi.org/10.1177/0363546512444554 CrossRefGoogle ScholarPubMed
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (2000). California Verbal Learning Test – second edition. Adult version. Manual. The Psychological Corporation. Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Holdnack, J. (2004). Reliability and validity of the Delis-Kaplan Executive Function System: An update. Journal of the International Neuropsychological Society, 10(2), 301–303. https://doi.org/10.1017/S1355617704102191 CrossRefGoogle ScholarPubMed
Devine, J.M. & Zafonte, R.D. (2009). Physical exercise and cognitive recovery in acquired brain injury: A review of the literature. PM and R, 1(6), 560–575. https://doi.org/10.1016/j.pmrj.2009.03.015 CrossRefGoogle ScholarPubMed
Dunn, A.L., Trivedi, M.H., Kampert, J.B., Clark, C.G., & Chambliss, H.O. (2005). Exercise treatment for depression: Efficacy and dose response. American Journal of Preventive Medicine, 28(1), 1–8. https://doi.org/10.1016/j.amepre.2004.09.003 CrossRefGoogle ScholarPubMed
Elliott, J., Jull, G., Noteboom, J.T., & Galloway, G. (2008). MRI study of the cross-sectional area for the cervical extensor musculature in patients with persistent whiplash associated disorders (WAD). Manual Therapy, 13(3), 258–265. https://doi.org/10.1016/j.math.2007.01.012 CrossRefGoogle Scholar
Ferguson, R.J., Mittenberg, W., Barone, D.F., & Schneider, B. (1999). Postconcussion syndrome following sports-related head injury: Expectation as etiology. Neuropsychology, 3(4), 582–529. https://doi.org/10.1037/0894-4105.13.4.582 CrossRefGoogle Scholar
Ferreira, A.F.B., Real, C.C., Rodrigues, A.C., Alves, A.S., & Britto, L.R.G. (2011). Short-term, moderate exercise is capable of inducing structural, bdnf-independent hippocampal plasticity. Brain Research, 1425, 111–122. https://doi.org/10.1016/j.brainres.2011.10.004 CrossRefGoogle ScholarPubMed
Finnoff, J.T., Peterson, V.J., Hollman, J.H., & Smith, J. (2009). Intrarater and Interrater Reliability of the Balance Error Scoring System (BESS). PM and R, 1(1), 50–54. https://doi.org/10.1016/j.pmrj.2008.06.002 CrossRefGoogle Scholar
Fogelman, D. & Zafonte, R. (2012). Exercise to enhance neurocognitive function after traumatic brain injury. PM and R, 4(11), 908–913. https://doi.org/10.1016/j.pmrj.2012.09.028 CrossRefGoogle ScholarPubMed
Giza, C.C. & Hovda, D.A. (2014). The new neurometabolic cascade of concussion. Neurosurgery, 4(4), S24–S33. https://doi.org/10.1227/NEU.0000000000000505 CrossRefGoogle Scholar
Golding, L. (2000). YMCA Fitness Testing and Assessment Manual (4th ed.). Champaign, Illinois: Human Kinetics Publishers, Inc.Google Scholar
Griesbach, G.S., Hovda, D.A., Molteni, R., Wu, A., & Gomez-Pinilla, F. (2004). Voluntary exercise following traumatic brain injury: Brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience, 125(1), 129–139. https://doi.org/10.1016/j.neuroscience.2004.01.030 CrossRefGoogle ScholarPubMed
Griesbach, G.S. (2011). Exercise after traumatic brain injury: Is it a double-edged sword? PM&R, 3(6S1), S64–S72. https://doi.org/10.1016/j.pmrj.2011.02.008 Google ScholarPubMed
Griesbach, G.S., Tio, D.L., Vincelli, J., McArthur, D.L., & Taylor, A.N. (2012). Differential effects of voluntary and forced exercise on stress responses after traumatic brain injury. Journal of Neurotrauma, 29(7), 1426–1433. https://doi.org/10.1089/neu.2011.2229 CrossRefGoogle ScholarPubMed
Griesbach, G.S., Hovda, D.A. & Gomez-Pinilla, F. (2009). Exercise-induced improvement in cognitive performance after traumatic brain injury in rats is dependent on BDNF activation. Brain Research, 1288, 105–115. https://doi.org/10.1016/j.brainres.2009.06.045 CrossRefGoogle ScholarPubMed
Gronwall, D. (1977). Paced auditory serial-addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367–373.CrossRefGoogle ScholarPubMed
Grool, A.M., Aglipay, M., Momoli, F., Meehan, W.P., Freedman, S.B., Yeates, K.O., … Zemek, R. (2016). Association between early participation in physical activity following acute concussion and persistent postconcussive symptoms in children and adolescents. Journal of the American Medical Association, 316(23), 2504–2514. https://doi.org/10.1001/jama.2016.17396 CrossRefGoogle ScholarPubMed
Halker, R.B. & Vargas, B.B. (2013). Primary exertional headache: Updates in the literature. Current Pain and Headache Reports, 17(6), 337. https://doi.org/10.1007/s11916-013-0337-8 CrossRefGoogle ScholarPubMed
Harris, P.A., Taylor, R., Thielke, R., Payne, J., Gonzalez, N., & Conde, J.G. (2009). Research electronic data capture (REDCap)–a metadata-driven methodology and workflow process for providing translational research informatics support. Journal of Biomedical Informatics, 42(2), 377–381. https://doi.org/0.1016/j.jbi.2008.08.010 CrossRefGoogle ScholarPubMed
Hays, R.D., Martin, S.A., Sesti, A.M., & Spritzer, K.L. (2005). Psychometric properties of the Medical Outcomes Study Sleep measure. Sleep Medicine, 6(1), 41–44. https://doi.org/10.1016/j.sleep.2004.07.006 Google ScholarPubMed
Heaton, R.K. (1981). A manual for the Wisconsin Card Sorting Test. Western Psychological Services. https://doi.org/10.1016/j.jns.2004.09.003 Google Scholar
Hilz, M.J., DeFina, P.A., Anders, S., Koehn, J., Lang, C.J., Pauli, E., … Marthol, H. (2011). Frequency analysis unveils cardiac autonomic dysfunction after mild traumatic brain injury. Journal of Neurotrauma, 28(9), 1727–1738. https://doi.org/10.1089/neu.2010.1497 CrossRefGoogle ScholarPubMed
Howell, D.R., Brilliant, A.N., Oldham, J.R., Berkstresser, B., Wang, F., & Meehan, W.P. (2020). Exercise in the first week following concussion among collegiate athletes: Preliminary findings. Journal of Science and Medicine in Sport, 23(2), 112–117. https://doi.org/10.1016/j.jsams.2019.08.294CrossRefGoogle ScholarPubMed
IBM Corp. (2016). IBM SPSS Statistics for Windows (V. 24.0).Google Scholar
Iverson, G.L., Gardner, A.J., Terry, D.P., Ponsford, J.L., Sills, A.K., Broshek, D.K., & Solomon, G.S. (2017). Predictors of clinical recovery from concussion: A systematic review. British Journal of Sports Medicine, 51(12), 941–948. https://doi.org/10.1136/bjsports-2017-097729 CrossRefGoogle ScholarPubMed
Iverson, G.L., Lange, R.T., Brooks, B.L., & Rennison, V.L.A. (2010). “Good old days” bias following mild traumatic brain injury. Clinical Neuropsychologist, 24(1), 17–37. https://doi.org/10.1080/13854040903190797 CrossRefGoogle ScholarPubMed
Julious, S.A. (2005). Sample size of 12 per group rule of thumb for a pilot study. Pharmaceutical Statistics. https://doi.org/10.1002/pst.185 CrossRefGoogle Scholar
Kamins, J., Bigler, E., Covassin, T., Henry, L., Kemp, S., Leddy, J.J., … Giza, C.C. (2017). What is the physiological time to recovery after concussion? A systematic review. British Journal of Sports Medicine, 51(12), 935–940. https://doi.org/10.1136/bjsports-2016-097464 Google ScholarPubMed
Kannel, W.B. & Sorlie, P. (1979). Some Health Benefits of Physical Activity: The Framingham Study. Archives of Internal Medicine, 139(8), 857–861. https://doi.org/10.1001/archinte.1979.03630450011006 CrossRefGoogle ScholarPubMed
Katz, D.A. & McHorney, C.A. (2002). The relationship between insomnia and health-related quality of life in patients with chronic illness. Journal of Family Practice, 51(3):229–235.Google ScholarPubMed
Kay, T., Harrington, D.E., Adams, R., Anderson, T., Berrol, S., Cicerone, K., … Malec, J. (1993). American congress of rehabilitation medicine: Definition of mild traumatic brain injury. The Journal of Head Trauma Rehabilitation, 8(3), 86–87. https://doi.org/10.1038/srep27921 Google Scholar
Kelly, M.E., Loughrey, D., Lawlor, B.A., Robertson, I.H., Walsh, C., & Brennan, S. (2014). The impact of exercise on the cognitive functioning of healthy older adults: A systematic review and meta-analysis. Ageing Research Reviews, 16, 12–31. https://doi.org/10.1016/j.arr.2014.05.002 CrossRefGoogle ScholarPubMed
Koo, T.K. & Li, M.Y. (2016). A guideline of selecting and reporting intraclass correlation coefficients for reliability research. Journal of Chiropractic Medicine, 15(2), 155–163. https://doi.org/10.1016/j.jcm.2016.02.012 CrossRefGoogle ScholarPubMed
Kreber, L.A. & Griesbach, G.S. (2016). The interplay between neuropathology and activity based rehabilitation after traumatic brain injury. Brain Research, 1640, 152–163. https://doi.org/10.1016/j.brainres.2016.01.016 CrossRefGoogle ScholarPubMed
Langdon, S., Königs, M., Adang, E.A.M.C., Goedhart, E., & Oosterlaan, J. (2020). Subtypes of sport-related concussion: A systematic review and meta-cluster analysis. Sports Medicine, 1–14. https://doi.org/10.1007/s40279-020-01321-9 Google ScholarPubMed
Lawrence, D.W., Richards, D., Comper, P., & Hutchison, M.G. (2018). Earlier time to aerobic exercise is associated with faster recovery following acute sport concussion. PLoS One, 13(4). https://doi.org/10.1371/journal.pone.0196062 CrossRefGoogle ScholarPubMed
Leddy, J.J., Haider, M.N., Ellis, M.J., Mannix, R., Darling, S.R., Freitas, M.S., … Willer, B. (2019). Early subthreshold aerobic exercise for sport-related concussion: A randomized clinical trial. JAMA Pediatrics, 173(4), 319–325. https://doi.org/10.1001/jamapediatrics.2018.4397 CrossRefGoogle ScholarPubMed
Leddy, J.J., Haider, M.N., Ellis, M., & Willer, B.S. (2018). Exercise is medicine for concussion. Current Sports Medicine Reports, 17(8), 262. https://doi.org/10.1249/JSR.0000000000000505 CrossRefGoogle ScholarPubMed
Lovell, M.R., Iverson, G.L., Collins, M.W., Podell, K., Johnston, K.M., Pardini, D., … Maroon, J.C. (2006). Measurement of symptoms following sports-related concussion: reliability and normative data for the post-concussion scale. Applied Neuropsychology, 13(3), 166–174. https://doi.org/10.1207/s15324826an1303_4 Google ScholarPubMed
Majerske, C.W., Mihalik, J.P., Ren, D., Collins, M.W., Reddy, C.C., Lovell, M.R., & Wagner, A.K. (2008). Concussion in sports: Postconcussive activity levels, symptoms, and neurocognitive performance. Journal of Athletic Training, 43(3), 265–274. https://doi.org/10.4085/1062-6050-43.3.265 CrossRefGoogle ScholarPubMed
McCrory, P, Meeuwisse, W.H., Aubry, M., Cantu, B., Dvorak, J., Echemendia, R.J., … Turner, M. (2013). Consensus statement on concussion in sport: The 4th International Conference on Concussion in Sport held in Zurich, November 2012. British Journal of Sports Medicine, 47(5), 250–258. http://bjsm.bmj.com/cgi/doi/10.1136/bjsports-2013-092313 CrossRefGoogle Scholar
McCrory, P, Meeuwisse, W., Johnston, K., Dvorak, J., Aubry, M., Molloy, M., & Cantu, R. (2009). Consensus statement on concussion in sport – The 3rd International Conference on concussion in sport, held in Zurich, November 2008. Journal of Clinical Neuroscience, 16, 755–755763.CrossRefGoogle Scholar
McCrory, P., Meeuwisse, W., Dvorak, J., Aubry, M., Bailes, J., Broglio, S., … Vos, P.E. (2017). Consensus statement on concussion in sport - The 5th International Conference on Concussion in Sport, held in Berlin. British Journal of Sports Medicine, 51(11), 838–847. https://doi.org/10.1136/bjsports-2017-097699 Google ScholarPubMed
Mittenberg, W., DiGiulio, D.V, Perrin, S., & Bass, A.E. (1992). Symptoms following mild head injury: Expectation as aetiology. Journal of Neurology, Neurosurgery & Psychiatry, 55, 200–204. https://doi.org/10.1136/jnnp.55.3.200 CrossRefGoogle ScholarPubMed
Moser, R., Iverson, G., Echemendia, R., Liovell, M., Schatz, P., Webbe, F., … Barth, J. (2007). Neuropsychological evaluation in the diagnosis and management of sports-related concussion⋆. Archives of Clinical Neuropsychology, 22(8), 909–916. https://doi.org/10.1016/j.acn.2007.09.004 CrossRefGoogle Scholar
Polinder, S., Cnossen, M.C., Real, R.G.L., Covic, A., Gorbunova, A., Voormolen, D.C., … Von Steinbuechel, N. (2018). A multidimensional approach to post-concussion symptoms in mild traumatic brain injury. Frontiers in Neurology, 9, 1113. https://doi.org/10.3389/fneur.2018.01113 CrossRefGoogle ScholarPubMed
Riemann, B.L. & Guskiewicz, K.M. (2000). Effects of mild head injury on postural stability as measured through clinical balance testing. Journal of Athletic Training, 35(1), 19.Google ScholarPubMed
Rockhill, C.M., Fann, J.R., Fan, M.Y., Hollingworth, W., & Katon, W.J. (2010). Healthcare costs associated with mild traumatic brain injury and psychological distress in children and adolescents. Brain Injury, 24(9), 1051–1060. https://doi.org/10.3109/02699052.2010.494586 CrossRefGoogle ScholarPubMed
Ruff, R.M., Niemann, H., Allen, C.C., Farrow, C.E., & Wylie, T. (1992). The ruff 2 and 7 selective attention test: A neuropsychological application. Perceptual and Motor Skills, 75(3_suppl), 1311–1319. https://doi.org/10.2466/pms.1992.75.3f.1311 CrossRefGoogle ScholarPubMed
Sackett, D.L., Straus, S.E., Richardson, W.S., Rosenberg, W.M.C., & Haynes, R.B. (2000). Evidence Based Medicine: How to Teach and Practice EBM. Edinburgh, UK: Churchill Livingston.Google Scholar
Sandoe, C.H. & Kingston, W. (2018). Exercise headache: A review. Current Neurology and Neuroscience Reports, 18(6), 28. https://doi.org/10.1007/s11910-018-0840-8 CrossRefGoogle ScholarPubMed
Silverberg, N.D. & Iverson, G.L. (2013). Is rest after concussion “the best medicine?” Recommendations for activity resumption following concussion in athletes, civilians, and military service members. Journal of Head Trauma Rehabilitation, 28(4), 250–259. https://doi.org/10.1097/htr.0b013e31825ad658 CrossRefGoogle ScholarPubMed
Spielberger, C.D., Gorsuch, R.L., & Lushene, R.E. (1970). STAI manual for the state-trait anxiety inventory. Self-Evaluation Questionnaire. https://doi.org/10.1037/t06496-000 Google Scholar
Tanaka, H., Monahan, K.D., & Seals, D.R. (2001). Age-predicted maximal heart rate revisited. Journal of the American College of Cardiology, 37(1), 153–156. https://doi.org/10.1016/S0735-1097(00)01054-8 CrossRefGoogle ScholarPubMed
Thomas, D.G., Apps, J.N., Hoffmann, R.G., McCrea, M., & Hammeke, T. (2015). Benefits of strict rest after acute concussion: A randomized controlled trial. Pediatrics, 135(2), 213–223. https://doi.org/10.1542/peds.2014-0966 CrossRefGoogle ScholarPubMed
Treleaven, J., Jull, G., & LowChoy, N. (2005). Smooth pursuit neck torsion test in whiplash-associated disorders: Relationship to self-reports of neck pain and disability, dizziness and anxiety. Journal of Rehabilitation Medicine, 37(4), 219–223. https://doi.org/10.1080/16501970410024299 Google ScholarPubMed
van Belle, G. (2011). Statistical rules of thumb (2nd ed.). In Statistical Rules of Thumb: Second Edition. https://doi.org/10.1002/9780470377963 CrossRefGoogle Scholar
Vanderbeken, I. & Kerckhofs, E. (2017). A systematic review of the effect of physical exercise on cognition in stroke and traumatic brain injury patients, NeuroRehabilitation, 40(1), 33–48. https://doi.org/10.3233/NRE-161388CrossRefGoogle ScholarPubMed
Voss, J.D., Connolly, J., Schwab, K.A., & Scher, A.I. (2015). Update on the epidemiology of concussion/mild traumatic brain injury. Current Pain and Headache Reports, 19(7), 32. https://doi.org/10.1007/s11916-015-0506-z CrossRefGoogle ScholarPubMed
Wechsler, D. (1997a). WAIS-III Administration and Scoring Manual. New York City, New York: The Psychological Corporation.Google Scholar
Wechsler, D. (1997b). Wechsler Memory Scale (3rd ed.). The Psychological Corporation.Google Scholar
Wise, E.K., Hoffman, J.M., Powell, J.M., Bombardier, C.H., & Bell, K.R. (2012). Benefits of exercise maintenance after traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 93(8), 1319–1323. https://doi.org/10.1016/j.apmr.2012.05.009 CrossRefGoogle ScholarPubMed
Yoon, K.J. & Kim, D.Y. (2018). Immediate effects of a single exercise on behavior and memory in the early period of traumatic brain injury in rats. Annals of Rehabilitation Medicine, 42(5), 643. https://doi.org/10.5535/arm.2018.42.5.643 CrossRefGoogle ScholarPubMed
Zafonte, R.D., Shih, S.L., Iaccarino, M.A., & Tan, C.O. (2018). Neurologic benefits of sports and exercise. Handbook of Clinical Neurology. https://doi.org/10.1016/B978-0-444-63954-7.00042-2 CrossRefGoogle ScholarPubMed
Supplementary material: File

Snyder et al. supplementary material

Snyder et al. supplementary material

Download Snyder et al. supplementary material(File)
File 786.1 KB