Cited by 20Traumatic Brain Injury ResearchLong-Term Effects of COVID-19Cognitive Functions and Memory

Neurocognitive and quality of life improvements associated with aerobic training for individuals with persistent symptoms after mild traumatic brain injury: secondary outcome analysis of a pilot randomized clinical trial

Open access
Gladstone, Emily, Narad, Megan E., Hussain, Fadhil, Quatman-Yates, Catherine C., Hugentobler, Jason, Wade, Shari L., Gubanich, Paul J., Kurowski, Brad G.·2019·Frontiers in Neurology

Abstract

OBJECTIVE: To report secondary neurocognitive and quality of life outcomes for a pilot randomized clinical trial (RCT) of aerobic training for management of prolonged symptoms after a mild traumatic brain injury (mTBI) in adolescents. SETTING: Outpatient research setting. PARTICIPANTS: Thirty adolescents between the ages of 12 and 17 years who sustained a mTBI and had between 4 and 16 weeks of persistent post concussive symptoms. DESIGN: Secondary outcome analysis of a partially masked RCT of sub-symptom exacerbation aerobic training compared with a full-body stretching program highlighting cognitive and quality of life outcomes MAIN MEASURES: The secondary outcomes assessed included neurocognitive changes in fluid and crystalized age-adjusted cognition using the National Institutes of Health (NIH) toolbox and self and parent-reported total quality of life using the Pediatric Quality of Life Inventory. RESULTS: Twenty-two percent of eligible participants enrolled in the trial. General linear models did not reveal statistically significant differences between groups. Within group analyses using paired t-tests demonstrated improvement in age-adjusted fluid cognition (t(13)=3.39, p=0.005, Cohen’s d=0.61) and crystalized cognition (t(13)=2.63, p=0.02, Cohen’s d=0.70) within the aerobic training group but no significant improvement within the stretching group. Paired t-tests demonstrated significant improvement in both self-reported and parent-reported total quality of life measures in the aerobic training group (self-report t(13)=3.51, p=0.004, Cohen’s d=0.94; parent-report t(13)=6.5, p<0.0001, Cohen’s d=1.80) and the stretching group (self-report t(14)=4.20, p=0.0009, Cohen’s d=1.08; parent-report t(14)=4.06, p=0.0012, Cohen’s d=1.045). CONCLUSION: Quality of life improved significantly in both the aerobic exercise and stretching groups; however, this study suggests that only sub-symptom exacerbation aerobic training was potentially beneficial for neurocognitive recovery, particularly the fluid cognition subset in the NIH Toolbox. Limited sample size and variation in outcomes measures limited ability to detect between group differences. Future research should focus on developing larger studies to determine optimal timing post injury and intensity of active rehabilitation to facilitate neurocognitive recovery and improve quality of life after mTBI. Trial Registration: NCT02035579

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fneur.2019.01002

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 43

  1. [1]Taylor CA Bell JM BM J Xu L. Traumatic brain injury–related emergency department visits, hospitalizations, and deaths—United States, 2007 and 2013. MMWR Surveill Summ. (2017) 66: 1– 18. 10.15585/mmwr.ss6609a1 28301451 PMC5829835 · DOI
  2. [2]Kirkwood MW Yeates KO Taylor HG Randolph C McCrea M Anderson VA. Management of pediatric mild traumatic brain injury: a neuropsychological review from injury through recovery. Clin Neuropsychol. (2008) 22: 769– 800. 10.1080/13854040701543700 17896204 PMC2847840 · DOI
  3. [3]Lumba-Brown A Yeates KO Sarmiento K Breiding MJ Haegerich TM Gioia GA. Centers for Disease Control and Prevention Guideline on the Diagnosis and Management of Mild Traumatic Brain Injury Among Children. JAMA Pediatr. (2018) 172: e182853. 10.1001/jamapediatrics.2018.2853 30193284 PMC7006878 · DOI
  4. [4]Choe MC Babikian T DiFiori J Hovda DA Giza CC. A pediatric perspective on concussion pathophysiology. Curr Opin Pediatr. (2012) 24: 689– 95. 10.1097/MOP.0b013e32835a1a44 23080130 · DOI
  5. [5]Barlow KM Crawford S Brooks BL Turley B Mikrogianakis A The incidence of postconcussion syndrome remains stable following mild traumatic brain injury in children. Pediatr Neurol. (2015) 23: 491– 7. 10.1016/j.pediatrneurol.2015.04.011 26421987 · DOI
  6. [6]Emery CA Barlow KM Brooks BL Max JE Villavicencio-Requis A Gnanakumar V. A systematic review of psychiatric, psychological, and behavioural outcomes following mild traumatic brain injury in children and adolescents. Can J Psychiatry. (2016) 61: 259– 69. 10.1177/0706743716643741 27254800 PMC4841286 · DOI
  7. [7]Barkhoudarian G Hovda DA Giza CC. The molecular pathophysiology of concussive brain injury–an update. Phys Med Rehabil Clin N Am. (2016) 27: 373– 93. 10.1016/j.pmr.2016.01.003 27154851 · DOI
  8. [8]Steenerson K Starling AJ. Pathophysiology of sports-related concussion. Neurol Clin. (2017) 35: 403– 8. 10.1016/j.ncl.2017.03.011 28673406 · DOI
  9. [9]Fogelman D Zafonte R. Exercise to enhance neurocognitive function after traumatic brain injury. PM R. (2012) 4: 908- 913. 10.1016/j.pmrj.2012.09.028 23174558 · DOI
  10. [10]Devine JM Zafonte RD. Physical exercise and cognitive recovery in acquired brain injury: a review of the literature. PM R. (2009) 1: 560– 75. 10.1016/j.pmrj.2009.03.015 19627946 · DOI
  11. [11]Kurowski BG Hugentobler J Quatman-Yates C Taylor J Gubanich P Altaye M. Aerobic exercise for adolescents with prolonged symptoms after mild traumatic brain injury: an exploratory randomized clinical trial. J Head Trauma Rehabil. (2017) 32: 79– 89. 10.1097/HTR.0000000000000238 27120294 PMC5081281 · DOI
  12. [12]Lal A Kolakowsky-Hayner SA Ghajar J Balamane M. The effect of physical exercise after a concussion: a systematic review and meta-analysis. Am J Sports Med. (2018) 46: 743– 52. 10.1177/0363546517706137 28570092 · DOI
  13. [13]Manikas V Babl FE Hearps S Dooley J Anderson V. Impact of exercise on clinical symptom report and neurocognition after concussion in children and adolescents. J Neurotrauma. (2017) 34: 1932– 8. 10.1089/neu.2016.4762 28228043 · DOI
  14. [14]Lawrence DW Richards D Comper P Hutchison MG. Earlier time to aerobic exercise is associated with faster recovery following acute sport concussion. PLoS ONE. (2018) 13: e0196062. 10.1371/journal.pone.0196062 29668716 PMC5905975 · DOI
  15. [15]Leddy JJ Haider MN Ellis MJ Mannix R Darling SR Freitas MS. Early subthreshold aerobic exercise for sport-related concussion: a randomized clinical trial. JAMA Pediatr. (2019) 173: 319– 25. 10.1001/jamapediatrics.2018.4397 30715132 PMC6450274 · DOI
  16. [16]Molteni R Ying Z Gomez-Pinilla F. Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray. Eur J Neurosci. (2002) 16: 1107– 16. 10.1046/j.1460-9568.2002.02158.x 12383240 · DOI · Paper page
  17. [18]Heaton RK Akshoomoff N Tulsky D Mungas D Weintraub S Dikmen S. Reliability and validity of composite scores from the NIH Toolbox Cognition Battery in adults. J Int Neuropsychol Soc. (2014) 20: 588– 98. 10.1017/S1355617714000241 24960398 PMC4103963 · DOI · Paper page
  18. [19]Varni JW Seid M Rode CA. The PedsQL: measurement model for the pediatric quality of life inventory. Med Care. (1999) 37: 126– 9. 10.1097/00005650-199902000-00003 10024117 · DOI · Paper page
  19. [20]Varni JW Seid M Kurtin PS. PedsQL 4.0: reliability and validity of the Pediatric Quality of Life Inventory version 4.0 generic core scales in healthy and patient populations. Med Care. (2001) 39: 800– 12. 10.1097/00005650-200108000-00006 11468499 · DOI · Paper page
  20. [21]Varni JW Burwinkle TM Seid M Skarr D. The PedsQL 4.0 as a pediatric population health measure: feasibility, reliability, and validity. Ambul Pediatr. (2003) 3: 329– 41. 10.1367/1539-4409(2003)003<0329:TPAAPP>2.0.CO;2 14616041 · DOI
  21. [22]McCarthy ML MacKenzie EJ Durbin DR Aitken ME Jaffe KM Paidas CN. The Pediatric Quality of Life Inventory: an evaluation of its reliability and validity for children with traumatic brain injury. Arch Phys Med Rehabil. (2005) 86: 1901– 9. 10.1016/j.apmr.2005.03.026 16213229 · DOI
  22. [23]McCarthy ML MacKenzie EJ Durbin DR Aitken ME Jaffe KM Paidas CN. Health-related quality of life during the first year after traumatic brain injury. Arch Pediatr Adolesc Med. (2006) 160: 252– 60. 10.1001/archpedi.160.3.252 16520444 · DOI
  23. [24]Rivara FP Vavilala MS Durbin D Temkin N Wang J O'Connor SS. Persistence of disability 24 to 36 months after pediatric traumatic brain injury: a cohort study. J Neurotrauma. (2012) 29: 2499– 504. 10.1089/neu.2012.2434 22757748 PMC3471122 · DOI
  24. [25]Aitken ME McCarthy ML Slomine BS Ding R Durbin DR Jaffe KM. Family burden after traumatic brain injury in children. Pediatrics. (2009) 123: 199– 206. 10.1542/peds.2008-0607 19117883 · DOI
  25. [26]Yuan W Wade SL Quatman-Yates C Hugentobler JA Gubanich PJ Kurowski BG. Structural connectivity related to persistent symptoms after mild tbi in adolescents and response to aerobic training: preliminary investigation. J Head Trauma Rehabil. (2017) 32: 378– 84. 10.1097/HTR.0000000000000318 28520668 PMC5668180 · DOI
  26. [27]Leppink J O'Sullivan P Winston K. Effect size - large, medium, and small. Perspect Med Educ. (2016) 5: 347– 9. 10.1007/s40037-016-0308-y 27752936 PMC5122517 · DOI
  27. [28]Shapiro S Wilk M An analysis of variance test for normality (complete samples). Biometrika. (1965) 52: 591– 611. 10.1093/biomet/52.3-4.591 · DOI · Paper page
  28. [29]Gagnon I Grilli L Friedman D Iverson GL. A pilot study of active rehabilitation for adolescents who are slow to recover from sport-related concussion. Scand J Med Sci Sports. (2016) 26: 299– 306. 10.1111/sms.12441 25735821 · DOI
  29. [30]Gauvin-Lepage J Friedman D Grilli L Sufrategui M De Matteo C Iverson GL. Effectiveness of an exercise-based active rehabilitation intervention for youth who are slow to recover after concussion. Clin J Sport Med. (2018). 10.1097/JSM.0000000000000634. [Epub ahead of print]. 30095507 · DOI
  30. [31]Swain RA Berggren KL Kerr AL Patel A Peplinski C Sikorski AM. On aerobic exercise and behavioral and neural plasticity. Brain Sci. (2012) 2: 709– 44. 10.3390/brainsci2040709 24961267 PMC4061809 · DOI
  31. [33]Majerske CW Mihalik JP Ren D Collins MW Reddy CC Lovell MR. Concussion in sports: postconcussive activity levels, symptoms, and neurocognitive performance. J Athl Train. (2008) 43: 265– 74. 10.4085/1062-6050-43.3.265 18523563 PMC2386420 · DOI
  32. [34]Whyte EF Gibbons N Kerr G Moran KA. Effect of a high-intensity, intermittent-exercise protocol on neurocognitive function in healthy adults: implications for return-to-play management after sport-related concussion. J Sport Rehabil. (2015) 24: 2014- 0201. 10.1123/jsr.2014-0201 25364978 · DOI
  33. [35]Pawlukiewicz A Yengo-Kahn AM Solomon G. The effect of pretest exercise on baseline computerized neurocognitive test scores. Orthop J Sports Med. (2017) 5: 2325967117734496. 10.1177/2325967117734496 29114564 PMC5656112 · DOI
  34. [36]Boyne P Dunning K Carl D Gerson M Khoury J Kissela B. High-intensity interval training in stroke rehabilitation. Top Stroke Rehabil. (2013) 20: 317– 30. 10.1310/tsr2004-317 23893831 · DOI
  35. [37]Boyne P Dunning K Carl D Gerson M Khoury J Rockwell B. High-intensity interval training and moderate-intensity continuous training in ambulatory chronic stroke: feasibility study. Phys Ther. (2016) 96: 1533– 44. 10.2522/ptj.20150277 27103222 PMC5046191 · DOI
  36. [38]Cipryan L Tschakert G Hofmann P. Acute and post-exercise physiological responses to high-intensity interval training in endurance and sprint athletes. J Sports Sci Med. (2017) 16: 219– 29. Available online at: http://www.jssm.org 28630575 PMC5465984
  37. [39]Dibble LE Hale TF Marcus RL Droge J Gerber JP LaStayo PC. High-intensity resistance training amplifies muscle hypertrophy and functional gains in persons with Parkinson's disease. Mov Disord. (2006) 21: 1444– 52. 10.1002/mds.20997 16773643 · DOI
  38. [40]Eddolls WTB McNarry MA Stratton G Winn CON Mackintosh KA. High-intensity interval training interventions in children and adolescents: a systematic review. Sports Med. (2017) 47: 2363– 74. 10.1007/s40279-017-0753-8 28643209 PMC5633633 · DOI
  39. [41]Hannan AL Hing W Simas V limstein M Coombes JS Jayasinghe R. High-intensity interval training versus moderate-intensity continuous training within cardiac rehabilitation: a systematic review and meta-analysis. Open Access J Sports Med. (2018) 9: 1- 17. 10.2147/OAJSM.S150596 29416382 PMC5790162 · DOI · Paper page
  40. [42]Hanssen H Minghetti A Magon S Anja Rossmeissl Athina Papadopoulou Christopher Klenk. Superior effects of high-intensity interval training vs. moderate continuous training on arterial stiffness in episodic migraine: a randomized controlled trial. Front Physiol. (2017) 8: 1086. 10.3389/fphys.2017.01086 29311997 PMC5742195 · DOI
  41. [43]Kelly NA Wood KH Allendorfer JB Ford MP Bickel CS Marstrander J. High-intensity exercise acutely increases substantia nigra and prefrontal brain activity in Parkinson's disease. Med Sci Monit. (2017) 23: 6064– 71. 10.12659/MSM.906179 29273705 PMC5747933 · DOI
  42. [44]Lucas SJ Cotter JD Brassard P Bailey DM. High-intensity interval exercise and cerebrovascular health: curiosity, cause, and consequence. J Cereb Blood Flow Metab. (2015) 35: 902– 11. 10.1038/jcbfm.2015.49 25833341 PMC4640257 · DOI
  43. [46]Thomas DG Apps JN Hoffmann RG McCrea M Hammeke T. Benefits of Strict rest after acute concussion: a randomized controlled trial. Pediatrics. (2015) 135: 213– 23. 10.1542/peds.2014-0966 25560444 · DOI

Authors
Gladstone, E., Narad, M. E., Hussain, F., Quatman-Yates, C. C., Hugentobler, J., Wade, S. L., Gubanich, P. J., & Kurowski, B. G.
Affiliations
  • MetroHealth (US)
  • Cincinnati Children's Hospital Medical Center (US)
  • University of Cincinnati (US)
Corresponding author
Kurowski, Brad G.
Venue
Frontiers in Neurology
Published
2019-09-18
Volume
10
Pages
1002-1002
ISSN
1664-2295 (ISSN-L)
OpenAlex
W2971840119
Cited by
20
References
2
Citations by year
2026: 2 · 2025: 7 · 2024: 2 · 2023: 7 · 2022: 2
FWCI
0.38
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Neurology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Cincinnati Children's Hospital Medical Center (UL1TR000077)
  • National Institutes of Health (UL1TR001425, UL1TR000077, TR000077)
  • National Center for Advancing Translational Sciences (TR000077)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (K23HD074683)
Topics
  • Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
  • Health Sciences › Medicine › Neurology › Long-Term Effects of COVID-19
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
Keywords
mild traumatic brain injury, post-concussion symptoms, aerobic exercise, adolescents, neurocognitive recovery, fluid cognition, quality of life, stretching, NIH Toolbox, PedsQL, exercise therapy, concussion rehabilitation, parent-reported outcomes, self-reported outcomes, NIH Toolbox Cognition Battery

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review