Subsymptomatic Aerobic Exercise for Patients With Postconcussion Syndrome: A Critically Appraised Topic

in Journal of Sport Rehabilitation

Clinical Scenario: Patients who experience prolonged concussion symptoms can be diagnosed with postconcussion syndrome (PCS) when those symptoms persist longer than 4 weeks. Aerobic exercise protocols have been shown to be effective in improving physical and mental aspects of health. Emerging research suggests that aerobic exercise may be useful as a treatment for PCS, where exercise allows patients to feel less isolated and more active during the recovery process. Clinical Question: Is aerobic exercise more beneficial in reducing symptoms than current standard care in patients with prolonged symptoms or PCS lasting longer than 4 weeks? Summary of Key Findings: After a thorough literature search, 4 studies relevant to the clinical question were selected. Of the 4 studies, 1 study was a randomized control trial and 3 studies were case series. All 4 studies investigated aerobic exercise protocol as treatment for PCS. Three studies demonstrated a greater rate of symptom improvement from baseline assessment to follow-up after a controlled subsymptomatic aerobic exercise program. One study showed a decrease in symptoms in the aerobic exercise group compared with the full-body stretching group. Clinical Bottom Line: There is moderate evidence to support subsymptomatic aerobic exercise as a treatment of PCS; therefore, it should be considered as a clinical option for reducing PCS and prolonged concussion symptoms. A previously validated protocol, such as the Buffalo Concussion Treadmill test, Balke protocol, or rating of perceived exertion, as mentioned in this critically appraised topic, should be used to measure baseline values and treatment progression. Strength of Recommendation: Level C evidence exists that the aerobic exercise protocol is more effective than the current standard of care in treating PCS.

Clinical Scenario

It is estimated that approximately 1.1 to 1.9 million sport-related concussions occur in patients 18 years or younger in the United States annually.1 Most adult patients who suffer from a concussion experience full relief from symptoms within 7 to 10 days of injury.2 However, approximately 10% to 20% of patients who sustain concussions experience symptoms that persist beyond this point. Patients who suffer from 3 or more symptoms, including headache, dizziness, fatigue, irritability, insomnia, concentration problems, or memory difficulty, for 4 or more weeks are diagnosed with postconcussion syndrome (PCS).3 Current recommendations for the treatment of concussions and PCS include physical and cognitive rest; however, this recommendation is vague, lacks evidence,4 and leaves a large degree of decision making up to the individual clinician. For a long time, it was believed that total rest until symptom resolution was the best practice for management of concussion and associated conditions. In recent years, there has been a shift in clinical treatment approaches that bring a more active recovery to the forefront of concussion management.58 These treatments vary based on the types of symptoms and deficits that persist after concussion.

Aerobic exercise protocols have been identified as a potentially beneficial treatment for individuals with persistent symptoms who are exacerbated by exertion. Prior research has used aerobic protocols to establish subsymptom baseline values.8 Patients are subjected to an initial aerobic protocol to establish the baseline symptomatic threshold. In the standard Balke Treadmill Concussion test, the baseline is determined by the patient reporting symptoms or unable to achieve full incline.5,9 In the studies included, there were minor variations in time and intensity utilized in the protocols.1013 These values are then used to develop active rehabilitation protocols for patients after concussion in which they complete aerobic activity at a subsymptomatic threshold of between 60% and 80% of the baseline threshold.1013

Clinical Question

Is aerobic exercise more beneficial in reducing symptoms than current standard care in patients with prolonged symptoms or PCS lasting longer than 4 weeks?

Summary of Search, “Best Evidence” Appraised, and Key Findings

  1. The literature was searched for studies that investigated whether an aerobic exercise protocol was more effective than the current standard of care for recovery from PCS.
  2. The literature search returned 17 possible studies related to the clinical question, of which 4 studies1013 met the inclusion criteria and were included.
  3. The 4 studies1013 included reported using aerobic exercise as a therapeutic intervention for PCS.
  4. Participants who completed controlled subsymptomatic aerobic exercise experienced a greater rate of symptom improvement from baseline assessment for follow-up.1013
  5. Subsymptomatic threshold can be determined through the Buffalo Concussion Treadmill test, Balke protocol, or Borg rating of perceived exertion (RPE). Patients with a concussion are not able to achieve maximum exertion. Symptom exacerbation occurs at a submaximum level.6,1214
  6. Athletes responded to subsymptomatic threshold training faster than nonathletes.13

Clinical Bottom Line

There is moderate evidence to support subsymptomatic aerobic exercise as a treatment of PCS; therefore, it should be considered as a clinical option for reducing PCS and prolonged concussion symptoms. Clinicians should use a previously validated protocol to determine subsymptomatic threshold, including the Buffalo Concussion Treadmill test, Balke protocol, and Borg RPE.6,1214 Although a specific timeline for duration of treatment has not been validated, there is evidence that 6 weeks of aerobic activity at 80% of subsymptom baseline may be effective in PCS treatment.1013 Clinicians should utilize an individualized plan of care that includes patient baseline scores and personalized progression based on subsymptomatic threshold values.

Strength of Recommendation

Level C evidence exists that aerobic exercise protocol is more effective than the current standard of care in treating PCS.

Search Strategy

Terms Used to Guide Search Strategy

  1. Patient/Client group: participants with PCS or prolonged symptoms
  2. Intervention/Assessment: aerobic exercise
  3. Comparison: current standard care
  4. Outcome(s): symptom improvement or readiness to return to activity
  5. Time: concussion symptoms lasting longer than 4 weeks

Sources of Evidence Searched

  1. The Cochrane Library
  2. MEDLINE
  3. CINAHL
  4. SPORTDiscus
  5. Additional resources obtained via review of reference lists and hand search

Inclusion and Exclusion Criteria

Inclusion Criteria

  1. Studies that investigated patients diagnosed with concussion or sport-related concussion
  2. Studies that investigated patients with PCS or prolonged symptoms lasting longer than 4 weeks
  3. Studies that investigated aerobic exercise as a therapeutic intervention
  4. Limited to English language
  5. Limited to the past 10 years (2008–2017)

Exclusion Criteria

  1. Studies that investigated pharmacological interventions for treatment of PCS
  2. Studies that investigated subsymptomatic aerobic exercise as a tool for determining readiness to return to activity

Results of Search

Four relevant studies1013 were located and categorized as shown in Table 1 (based on Levels of Evidence).15 Of the 4 studies identified, 3 studies are case series and 1 study is a randomized control trial.

Table 1

Summary of Study Designs of Articles Retrieved

Level of evidenceStudy designNumber locatedReferences
1bRandomized control trial1Kurowski et al12
4Case series3Leddy et al,13 Gagnon et al11, and Chrisman et al10

Best Evidence

The studies in Table 2 were identified as the best evidence and selected for inclusion in this critically appraised topic. These studies were selected because they explored aerobic exercise as treatment for PCS.

Table 2

Characteristics of Included Studies

Leddy et al13Chrisman et al10Kurowski et al12Gagnon et al11
Study designCase seriesCase seriesRandomized clinical trialCase series
Participants13 participants recruited from Buffalo Concussion Clinic with PCS83 participants from Seattle Children’s Hospital, youth diagnosed with a concussion and symptoms lasting longer than 4 wk30 adolescents with mild TBI10 participants with sport-related concussion
Mean age was 27.9 (14.3) yMean age was 14.9 (2.3) y oldAge = 12–17 yAge = 14–18 y
Inclusion criteria: (1) Prolonged symptoms at rest for greater than or equal to 6 wk; (2) Had symptom exacerbation during 2 graded treadmill exercise tests; and (3) Low cardiac riskInclusion criteria: (1) Seen for concussion >1 mo but <300 d after their concussion; (2) Completed Balke treadmill test; and (3) Seen by a physical therapist in the SSTEP program at least twiceInclusion criteria: (1) Presence of at least 3 of 8 symptoms of PCS; (2) Exacerbation of symptoms with physical activity; and (3) Persistent symptoms lasting longer than 4 wkInclusion criteria: (1) Persistent symptoms lasting longer than 4 wk; and (2) Adolescents with sport-related concussion
Exclusion criteria: (1) Lived too far from clinic; (2) Psychiatric diagnosis; (3) Injury occurred more than 1 y ago; (4) Cervical disk herniation; and (5) Inability to understand EnglishNo exclusion criteria were givenExclusion criteria: (1) Severe TBI; (2) Taking medications or other physical therapy as treatment; (3) Preexisting cognitive disorders; and (4) Preexisting cardiovascular problemsExclusion criteria: Coexisting cervical, oculomotor, and/or vestibular impairments
6 participants were identified as athletes76% of concussions were sport-related concussions
6 participants were identified as having a prior concussion
Intervention investigatedParticipants performed a treadmill exercise test using the Balke protocol until symptom exacerbationParticipants performed a treadmill exercise test using the Balke protocol until symptom exacerbationParticipants performed an aerobic bike test, assessing Borg RPE and increasing intensity every 5 minParticipants completed a 4-part rehabilitation program for 6 wk: (1) Submaximal aerobic training for 15 min; (2) Coordination exercises; (3) Visualization and imagery; and (4) Daily home exercises
Symptoms: Heart rate and blood pressure were recorded to determine thresholdSymptoms: Heart rate and blood pressure were recorded to determine thresholdIntensity increased until the participant reached 30 min or RPE of 1660% of maximum heart rate was determined by calculating maximum heart rate with the 220-age formula
Participants performed aerobic exercise for the same duration as the prior treadmill test at 80% of the maximum treadmill heart rate at a frequency of once per day for 5 or 6 d of the weekParticipants performed daily aerobic exercise at the same heart rate level as baseline for 20 minThe intervention group performed the aerobic biking at 80% of the initial bike test for 5 or 6 times per week for 6 wk. The stretching groups completed a full-body stretching program with new stretches each weekParticipants had a choice between walking/light jogging or stationary bicycle for the aerobic activity
Outcome measure(s)(1) Symptoms

(2) Maximum heart rate

(3) Systolic blood pressure

(4) Diastolic blood pressure

(5) Achievement of maximal exertion
(1) Symptoms (type, severity, and duration)

(2) Maximum heart rate

(3) Systolic blood pressure

(4) Diastolic blood pressure

(5) Exercise duration
(1) Symptoms (type and severity)

(2) RPE

(3) Adherence to program
(1) Symptoms

(2) Mood and energy level
Main findingsAfter 3 mo, 10 out of 12 participants reported to be symptom free at restDuration and severity of symptoms decreased as shown in SCAT 2 scoresThe subsymptomatic exacerbation aerobic training group experienced greater rate of improvement than the full-body stretching groupParticipants’ symptoms scores significantly decreased from baseline to 6-wk follow-up
Symptom total was a mean of 9.67 (5.87) at baseline and 5.42 (4.54) at follow-up; P = .002Mean SCAT 2 scores:

Baseline <6 wk = 36.3, SE = 3.68

Baseline 6–12 wk = −5.58, SE = 5.23

Baseline >12 wk = 10.0, SE = 6.07
At baseline, the aerobic training group had a mean symptom score of 37.4 and the stretching group had a mean symptom score of 40.3Symptom total was a mean of 17.4 (12.3) at baseline and 2.7 (3.2) at 6-wk follow-up; P = .004
Exercise time improved from baseline at 9.75 (6.73) min to 18.67 (2.53) minNone of the participants experienced worsening of symptomsAfter final assessment, aerobic training group has a mean symptom score of 4.17 and stretching group 15.93; P = .04Treatment duration lasted 6.8 (4.7) wk
Athletes responded to subsymptomatic threshold exercise training faster than nonathletes
Level of evidence441b4
Validity score (if applicable)N/AN/APEDro score: 9/10N/A
ConclusionControlled subsymptomatic threshold exercise was beneficial in decreasing symptoms of PCSAerobic exercise decreased PCS symptoms exponentiallySubsymptomatic aerobic exercise was more beneficial in decreasing PCS symptoms than full-body stretchingAerobic exercise program greatly reduced PCS symptoms
Participants who completed controlled subsymptomatic threshold exercise had a decrease in symptoms of PCS from baseline to follow-up at 3 moParticipants continued the Balke Treadmill Concussion test until total symptom resolutionParticipants who completed the subsymptomatic exacerbation aerobic exercise protocol experienced a greater rate of symptom improvement than the full-body stretching groupIn these participants who complete the aerobic exercise program, symptoms improved from baseline to follow-up at 6 wk
Further research should include assessment of cognitive performanceFurther research needs to follow recovery time

Abbreviations: PCS, postconcussion syndrome; TBI, traumatic brain injury; RPE, rating of perceived exertion; SSTEP, subsymptom threshold exercise program; SCAT, Sport Concussion Assessment Tool; N/A, not applicable.

Implications for Practice, Education, and Future Research

Several therapeutic interventions have been recommended for patients who have prolonged recovery after sustaining a concussion.8 This review proposed aerobic exercise as a comparison to the current standard of care and found that there is moderate evidence to support subsymptomatic aerobic exercise as a treatment of PCS. Because of current limitations in the literature, it is important that clinicians use sound clinical judgment when implementing this treatment. Three of the 4 studies included in this paper are case series that lack external validity due to their lack of a control group and limited generalizability to other populations. However, there is sound theoretical evidence that this treatment may help some patients with PCS. Despite the limitations of the available research, we believe that the consistent positive results warrant utilization of such a protocol for patients suffering from PCS.

In patients who suffer from PCS and prolonged symptoms, 3 or more of the following symptoms are included: headache, dizziness, fatigue, irritability, insomnia, concentration problems, or memory difficulty; current recommendations suggest preliminary evidence is available to support the implementation of controlled subsymptomatic aerobic exercise.7,8 The subsymptomatic threshold should be determined using a validated measure like the Buffalo Concussion Treadmill test, Balke protocol, or Borg RPE. All 4 studies identified a treatment period of 6 to 9 weeks, with daily treatment at the subsymptomatic level that was predetermined through baseline testing. Three of the studies10,11,13 suggested daily aerobic exercise should last 15 to 20 minutes, and the other study12 required 30 minutes. By determining subsymptomatic threshold, patients can participate in subsymptomatic aerobic exercise to tolerance. This coincides with current concussion management recommendations, which focus on avoiding symptom exacerbation.7,16

Furthermore, there are emotional benefits of exercise as treatment of PCS. Exercise gives patients increased self-efficacy; less anxiety, stress, and depression; and better overall well-being.1719 Regular exercise has shown to have cognitive benefits in improving cognitive function, sleep, learning, and memory.17,18 Athletes, who are conditioned to an active lifestyle, may be at risk of feeling isolated and removed during concussion recovery. An active approach to their rehabilitation might help improve overall cognitive function, decrease depression and isolation, and restore an active lifestyle that will help to promote healing.20 Leddy et al13 found that athletes responded to the aerobic exercise program faster than nonathletes, suggesting that aerobic exercise was beneficial specifically for athletes.

Although the current evidence for using submaximal exercise is promising, the level of evidence is low due to study design, number of participants, and population. However, a recent systematic review identified that it may be beneficial.8 Further research should include randomized controlled trials with large sample sizes and uniform control measures. Only 1 study identified the participants as having sport-related concussion,11 whereas 2 other studies identified and compared the participants’ mechanism of injury as sport-related concussion or another mechanism.10,13 More research should be completed with a focus on individual populations, such as sport-related concussion, as there may be benefit of aerobic activity in those active prior to the injury.20

This critically appraised topic should be reviewed in 2 years, or when additional best evidence becomes available, to determine whether additional best evidence has been published that may change the clinical bottom line for the research question posed in this review.

Acknowledgments

There were no sources of funding to support this critically appraised topic. There are no conflicts of interest directly related to this critically appraised topic.

References

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    Bryan MARowhani-Rahbar AComstock RDRivara F; Seattle Sports Concussion Research Collaborative. Sports- and recreation-related concussions in US youth. Pediatrics. 2016;138(1):20154635. PubMed ID: 27325635 doi:10.1542/peds.2015-4635

    • Crossref
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    McCrory PMeeuwisse WHAubry Met al. Consensus statement on concussion in sport: the 4th international conference on concussion in sport held in Zurich, November 2012. Br J Sports Med. 2013;47(5):250258. PubMed ID: 23479479 doi:10.1136/bjsports-2013-092313

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    Boake CMcCauley SRLevin HSet al. Diagnostic criteria for postconcussional syndrome after mild to moderate traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2005;17(3):350356. PubMed ID: 16179657 doi:10.1176/jnp.17.3.350

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  • 4.

    Silverberg NDIverson GL. Is rest after concussion “the best medicine?”: recommendations for activity resumption following concussion in athletes, civilians, and military service members. J Head Trauma Rehabil. 2013;28(4):250259. PubMed ID: 22688215 doi:10.1097/HTR.0b013e31825ad658

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    Ellis MJLeddy JWiller B. Multi-disciplinary management of athletes with post-concussion syndrome: an evolving pathophysiological approach. Front Neurol. 2016;7:136. PubMed ID: 27605923 doi:10.3389/fneur.2016.00136

    • Crossref
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  • 6.

    Leddy JJWiller B. Use of graded exercise testing in concussion and return-to-activity management. Curr Sports Med Rep. 2013;12(6):370376. PubMed ID: 24225521 doi:10.1249/JSR.0000000000000008

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    McCrory PMeeuwisse WDvorak Jet al. Consensus statement on concussion in sport-the 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. 2017;51(11):838847. PubMed ID: 28446457 doi:10.1136/bjsports-2017-097699

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  • 8.

    Schneider KJLeddy JJGuskiewicz KMet al. Rest and treatment/rehabilitation following sport-related concussion: a systematic review. Br J Sports Med. 2017;51:930934. PubMed ID: 28341726 doi:10.1136/bjsports-2016-097475

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  • 9.

    Darling SRLeddy JJBaker JGet al. Evaluation of the Zurich guidelines and exercise testing for return to play in adolescents following concussion. Clin J Sport Med. 2014;24(2):128133. PubMed ID: 24184849 doi:10.1097/JSM.0000000000000026

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  • 10.

    Chrisman SPWhitlock KBSomers Eet al. Pilot study of the sub-symptom threshold exercise program (SSTEP) for persistent concussion symptoms in youth. NeuroRehabilitation. 2017;40:493499. PubMed ID: 28222566 doi:10.3233/NRE-161436

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Gagnon IGrilli LFriedman DIverson 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(3):299306. PubMed ID: 25735821 doi:10.1111/sms.12441

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Kurowski BGHugentobler JQuatman-Yates Cet al. Aerobic exercise for adolescents with prolonged symptoms after mild traumatic brain injury: an exploratory randomized clinical trial. J Head Trauma Rehabil. 2017;32(2):7989. PubMed ID: 27120294 doi:10.1097/HTR.0000000000000238

    • Crossref
    • PubMed
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    • Export Citation
  • 13.

    Leddy JJKozlowski KDonnelly JPPendergast DREpstein LHWiller B. A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clin J Sport Med. 2010;20(1):2127. PubMed ID: 20051730 doi:10.1097/JSM.0b013e3181c6c22c

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Leddy JJBaker JGKozlowski KBisson LWiller B. Reliability of a graded exercise test for assessing recovery from concussion. Clin J Sport Med. 2011;21(2):8994. PubMed ID: 21358497 doi:10.1097/JSM.0b013e3181fdc721

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    OCEBM Levels of Evidence Working Group. The Oxford 2011 Levels of Evidence. Oxford Centre for Evidence-Based Medicine. 2011. http://www.cebm.net/index.aspx?o=5653

    • Export Citation
  • 16.

    McLeod TCVGioia GA. Cognitive rest: the often neglected aspect of concussion management. Athl Ther Today. 2010;15(2):13. doi:10.1123/att.15.2.1

  • 17.

    Hogan CLCatalino LIMata JFredrickson BL. Beyond emotional benefits: physical activity and sedentary behaviour affect psychosocial resources through emotions. Psychol Health. 2015;30(3):354369. PubMed ID: 25307453 doi:10.1080/08870446.2014.973410

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    McKee ACDaneshvar DHAlvarez VEStein TD. The neuropathology of sport. Acta Neuropathol. 2014;127(1):2951. PubMed ID: 24366527 doi:10.1007/s00401-013-1230-6

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Rasmussen LJustice DChang KWNelson VSYang LJ. Home exercise DVD promotes exercise accuracy by caregivers of children and adolescents with brachial plexus palsy. PM R. 2013;5(11):924930. PubMed ID: 23770351 doi:10.1016/j.pmrj.2013.06.003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Mychasiuk RHehar HMa ICandy SEsser MJ. Reducing the time interval between concussion and voluntary exercise restores motor impairment, short-term memory, and alterations to gene expression. Eur J Neurosci. 2016;44(7):24072417. PubMed ID: 27521273 doi:10.1111/ejn.13360

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

The authors are with Athletic Training Program, A.T. Still University, Mesa, AZ. Ritter is also with Athletic Training Program, Department of Interdisciplinary Health Sciences, Arizona School of Heath Sciences, A.T. Still University, Mesa, AZ.

Ritter (kritter@atsu.edu) is corresponding author.
Journal of Sport Rehabilitation
Article Sections
References
  • 1.

    Bryan MARowhani-Rahbar AComstock RDRivara F; Seattle Sports Concussion Research Collaborative. Sports- and recreation-related concussions in US youth. Pediatrics. 2016;138(1):20154635. PubMed ID: 27325635 doi:10.1542/peds.2015-4635

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    McCrory PMeeuwisse WHAubry Met al. Consensus statement on concussion in sport: the 4th international conference on concussion in sport held in Zurich, November 2012. Br J Sports Med. 2013;47(5):250258. PubMed ID: 23479479 doi:10.1136/bjsports-2013-092313

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Boake CMcCauley SRLevin HSet al. Diagnostic criteria for postconcussional syndrome after mild to moderate traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2005;17(3):350356. PubMed ID: 16179657 doi:10.1176/jnp.17.3.350

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Silverberg NDIverson GL. Is rest after concussion “the best medicine?”: recommendations for activity resumption following concussion in athletes, civilians, and military service members. J Head Trauma Rehabil. 2013;28(4):250259. PubMed ID: 22688215 doi:10.1097/HTR.0b013e31825ad658

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Ellis MJLeddy JWiller B. Multi-disciplinary management of athletes with post-concussion syndrome: an evolving pathophysiological approach. Front Neurol. 2016;7:136. PubMed ID: 27605923 doi:10.3389/fneur.2016.00136

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Leddy JJWiller B. Use of graded exercise testing in concussion and return-to-activity management. Curr Sports Med Rep. 2013;12(6):370376. PubMed ID: 24225521 doi:10.1249/JSR.0000000000000008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    McCrory PMeeuwisse WDvorak Jet al. Consensus statement on concussion in sport-the 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. 2017;51(11):838847. PubMed ID: 28446457 doi:10.1136/bjsports-2017-097699

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Schneider KJLeddy JJGuskiewicz KMet al. Rest and treatment/rehabilitation following sport-related concussion: a systematic review. Br J Sports Med. 2017;51:930934. PubMed ID: 28341726 doi:10.1136/bjsports-2016-097475

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Darling SRLeddy JJBaker JGet al. Evaluation of the Zurich guidelines and exercise testing for return to play in adolescents following concussion. Clin J Sport Med. 2014;24(2):128133. PubMed ID: 24184849 doi:10.1097/JSM.0000000000000026

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Chrisman SPWhitlock KBSomers Eet al. Pilot study of the sub-symptom threshold exercise program (SSTEP) for persistent concussion symptoms in youth. NeuroRehabilitation. 2017;40:493499. PubMed ID: 28222566 doi:10.3233/NRE-161436

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Gagnon IGrilli LFriedman DIverson 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(3):299306. PubMed ID: 25735821 doi:10.1111/sms.12441

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Kurowski BGHugentobler JQuatman-Yates Cet al. Aerobic exercise for adolescents with prolonged symptoms after mild traumatic brain injury: an exploratory randomized clinical trial. J Head Trauma Rehabil. 2017;32(2):7989. PubMed ID: 27120294 doi:10.1097/HTR.0000000000000238

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Leddy JJKozlowski KDonnelly JPPendergast DREpstein LHWiller B. A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clin J Sport Med. 2010;20(1):2127. PubMed ID: 20051730 doi:10.1097/JSM.0b013e3181c6c22c

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Leddy JJBaker JGKozlowski KBisson LWiller B. Reliability of a graded exercise test for assessing recovery from concussion. Clin J Sport Med. 2011;21(2):8994. PubMed ID: 21358497 doi:10.1097/JSM.0b013e3181fdc721

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    OCEBM Levels of Evidence Working Group. The Oxford 2011 Levels of Evidence. Oxford Centre for Evidence-Based Medicine. 2011. http://www.cebm.net/index.aspx?o=5653

    • Export Citation
  • 16.

    McLeod TCVGioia GA. Cognitive rest: the often neglected aspect of concussion management. Athl Ther Today. 2010;15(2):13. doi:10.1123/att.15.2.1

  • 17.

    Hogan CLCatalino LIMata JFredrickson BL. Beyond emotional benefits: physical activity and sedentary behaviour affect psychosocial resources through emotions. Psychol Health. 2015;30(3):354369. PubMed ID: 25307453 doi:10.1080/08870446.2014.973410

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    McKee ACDaneshvar DHAlvarez VEStein TD. The neuropathology of sport. Acta Neuropathol. 2014;127(1):2951. PubMed ID: 24366527 doi:10.1007/s00401-013-1230-6

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Rasmussen LJustice DChang KWNelson VSYang LJ. Home exercise DVD promotes exercise accuracy by caregivers of children and adolescents with brachial plexus palsy. PM R. 2013;5(11):924930. PubMed ID: 23770351 doi:10.1016/j.pmrj.2013.06.003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Mychasiuk RHehar HMa ICandy SEsser MJ. Reducing the time interval between concussion and voluntary exercise restores motor impairment, short-term memory, and alterations to gene expression. Eur J Neurosci. 2016;44(7):24072417. PubMed ID: 27521273 doi:10.1111/ejn.13360

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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