Skip to main content
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2017 Dec 1.
Published in final edited form as: Neurosurgery. 2016 Dec;79(6):912–929. doi: 10.1227/NEU.0000000000001447

Concussion is Treatable: Statements of Agreement from the Targeted Evaluation and Active Management (TEAM) Approaches to Treating Concussion Meeting held in Pittsburgh, October 15–16, 2015

Michael W Collins 1, Anthony P Kontos 1, David O Okonkwo 2, Jon Almquist 3, Julian Bailes 4, Mark Barisa 5, Jeffrey Bazarian 6, O Josh Bloom 7, David Brody 8, Robert Cantu 9, Javier Cardenas 10, Jay Clugston 11, Randall Cohen 12, Ruben Echemendia 13, RJ Elbin 14, Richard Ellenbogen 15, Janna Fonseca 7, Gerard Gioia 16, Kevin Guskiewicz 17, Robert Heyer 18, Gillian Hotz 19, Grant L Iverson 20, Barry Jordan 21, Geoffrey Manley 22, Joseph Maroon 2, Thomas McAllister 23, Michael McCrea 24, Anne Mucha 25, Elizabeth Pieroth 26, Kenneth Podell 27, Matthew Pombo 28, Teena Shetty 29, Allen Sills 30, Gary Solomon 30, Danny G Thomas 24,31, Tamara C Valovich McLeod 32, Tony Yates 33, Ross Zafonte 20
PMCID: PMC5119544  NIHMSID: NIHMS818694  PMID: 27741219

Abstract

Background

Conventional management for concussion involves prescribed rest and progressive return to activity. Recent evidence challenges this notion and suggests that active approaches may be effective for some patients. Previous concussion consensus statements provide limited guidance regarding active treatment.

Objective

To describe the current landscape of treatment for concussion and provide summary agreements related to treatment in order to assist clinicians in the treatment of concussion.

Methods

On October 14–16, 2015, the Targeted Evaluation & Active Management (TEAM) Approaches To Treating Concussion meeting was convened in Pittsburgh, Pennsylvania, USA. 37 concussion experts from neuropsychology, neurology, neurosurgery, sports medicine, physical medicine and rehabilitation, physical therapy, athletic training, and research, and 12 individuals representing sport, military, and public health organizations attended the meeting. The 37 experts indicated their agreement on a series of statements using an audience response system clicker device.

Results

A total of 16 statements of agreement were supported covering: 1) Summary of the Current Approach to Treating Concussion, 2) Heterogeneity and Evolving Clinical Profiles of Concussion, 3) Targeted Evaluation and Active Management Approach to Concussion Treatment: Specific Strategies, and 4) Future Directions: A Call to Research. Support (ie, response of agree or somewhat agree) for the statements ranged from to 97–100%.

Conclusion

Concussions are characterized by diverse symptoms and impairments and evolving clinical profiles; recovery varies based on modifying factors, injury severity, and treatments. Active and targeted treatments may enhance recovery following concussion. Research is needed on concussion clinical profiles, biomarkers, and the effectiveness and timing of treatments.

BACKGROUND

The Centers for Disease Control and Prevention (CDC) have labeled concussion a major public health issue due to acute and potential long term effects associated with this injury. Sport and recreation related concussions (SRC) in particular have increased in incidence, with approximately 1.6 to 3.8 million SRCs occurring every year in the U.S.1 Emergency department visits for SRC doubled between 1997 and 2007 for children 8 to 13 years and increased 200% for adolescents 14 to 19 years of age.2 Recent epidemiological studies document increases in the reported incidence rates for SRC at both college and high school levels.3 Knowledge about concussion has increased significantly over the past decade with respect to the definition of signs and symptoms,4 assessment approaches,5 risk factors,610 and prognosis.11,12 However, the treatment and management of concussion has received little attention in the literature during this time period. This progression is a natural phenomenon in medicine, with the initial phase focusing largely on the definition of the condition and its identification/diagnosis, followed by a later focus on its treatment.13 The limited research related to treatment has focused on the effectiveness of prescribed cognitive and physical rest,14,15 Moreover, the approach to treating and managing concussion is largely a uniform approach based on a conceptual framework as a homogeneous injury.16 This is surprising given that current consensus statements highlight the individualized nature of concussion.17 In short, many clinicians are treating patients with concussion much the same way today as they did a decade ago: using a rest based approach.

The notion of treating a concussion more actively than prescribed rest is also not recognized by the public. In fact, in a recent Harris Poll, a majority (71%) of over 2,000 U.S. adults surveyed did not recognize that concussions are treatable.18 In this same report, 1 in 3 adults reported that their child received no prescribed treatment following a concussion. Among those receiving treatment, the most commonly reported treatments were prescribed rest (51%), hydration (34%), and over the counter medicine (28%).18

OBJECTIVES

The preceding findings underscore the need to better align clinical practice with emerging concussion research. To that end, a group of concussion experts was convened October 14–16, 2015 in Pittsburgh, Pennsylvania to determine areas of agreement regarding the current state of concussion treatment. In the current paper, we present the results of this 2-day effort. This paper is designed to foster an understanding among clinicians, scientists, as well as lay people that concussion symptoms and impairment are treatable using more active and targeted approaches than prescribed rest alone. The agreement statements that emerged from this meeting may be useful in guiding the treatment of concussions that result from a variety of causes including sport and recreational activities, motor vehicle collisions, falls, assaults, and those occurring during military service. It is important to note that the focus of the current meeting, this paper, and concomitant statements was on agreement and not consensus, per se. In contrast to meetings such as the 4th International Conference on Concussion, which employed formal consensus meeting guidelines from the Consensus Development Program in the Office of Disease Prevention of the US National Institutes of Health (NIH)-which have since been retired by the NIH, the current meeting employed a majority voting approach to determining agreement on each statement. We employed a method of voting similar to that used by Smith and colleagues (see Methods section below for additional information).19

PURPOSE

The primary purpose of the current paper is to review the current state of treatment for concussion and provide summary agreements to assist clinicians in the treatment of this injury. Additional purposes of the paper are to: 1) summarize current expert consensus and empirical gaps in the research related to treating concussion; 2) present and describe clinical approaches to conceptualizing and classifying concussion; 3) discuss targeted evaluation and active management approaches for treating concussion; and 4) identify key areas regarding concussion treatment that require further research and support. For both the meeting and paper, the term concussion was defined per the 4th International Conference on Concussion.17 The current paper was intended to build on previous statements that provide guidelines for definitions, signs/symptoms, evaluation, return to play (RTP), and other issues related to concussion. The reader is therefore referred to the papers discussed later in this paper for additional information about these topics. The paper is organized into 4 primary sections that reflect the content of the presentations and focus of the meeting. The 4 sections include: 1) Summary of the Current Approach to Treating Concussion, 2) Heterogeneity and Evolving Clinical Profiles of Concussion, 3) Targeted Evaluation and Active Management Approach to Concussion Treatment: Specific Strategies, and 4) Future Directions: A Call to Research.

METHODS

For the reasons outlined above, on October 14–16, 2015, the Targeted Evaluation & Active Management (TEAM) Approaches To Treating Concussion meeting was convened in Pittsburgh, Pennsylvania, USA. The meeting was supported through grants from the National Football League and University of Pittsburgh Medical Center. Neither organization influenced the content of the meeting or this paper. Concussion experts from neuropsychology, neurology, neurosurgery, sports medicine, physical medicine and rehabilitation, physical therapy, athletic training, and research (referred to as “authors” throughout this document); as well as individuals representing sports, the military, and public health organizations (referred to as “participants” throughout this document) attended the meeting. A total of 38 authors, representing 33 clinical and academic institutions, and 14 participants, representing 12 sport, military, and public health organizations, attended the meeting. Prior to the meeting, the statements of agreement, along with supporting information and references, were drafted by the primary authors and circulated to contributing authors for review and comment. All primary authors, contributing authors, and invited participants were required to sign an International Committee of Medical Journal Editors (ICMJE) Form for Disclosure of Potential Conflicts of Interest. Detailed information related to each author’s affiliations and conflicts of interests are available in the Appendix.

Following an initial day of presentations by experts in the relevant areas and discussion of this paper with the author and participants, key statements of agreement were voted on, evaluated, and revised by the authors. During the month following the meeting, authors were assigned (by the primary authors based on expertise and meeting group assignments) in groups of 2–3 to develop 1–2 statements of agreement and subsequently revise a supporting section. After 2 rounds of revisions with authors, the primary authors edited and compiled a final paper that was then reviewed and approved by all primary and contributing authors.

Determining Agreement for Each Statement

Each of the authors was provided with an audience response system (ARS) clicker device to register their agreement level with each statement. Invited participants, though active in the meeting and discussions of each statement of agreement, were not provided with ARS devices in order to avoid conflicts with their positions within their representative organizations. The ARS devices were tested prior to each session to make sure they were working correctly. Following topical presentations and a panel discussion related to each statement of agreement, authors indicated their agreement with each statement using a 1-disagree, 2-somewhat disagree, 3-somewhat agree, or 4-agree point Likert-type response scale. All statements of agreement for a particular section were voted on prior to revealing the results to the audience. All votes were anonymous and a summary of group response data for each item was provided to all authors and invited participants immediately following the conclusion of voting in each section. The authors and invited participants discussed each statement of agreement and vote in an open forum. During these open forum discussions, authors were able to propose new statements of agreement for consideration. At this time, statements were revised based on suggestions and feedback from the authors and invited participants. These revisions and any newly proposed statements were discussed further during breakout sessions that included authors representing each of the sections of the paper (see section author list). Statements that received greater than 50% combined “disagree” and “somewhat disagree” ratings or those that were unclear were revised for a second vote. However, voting results indicated that none of the statements of agreement met the preceding criteria. The voting sessions were open only to authors. Subsequent to all revisions as agreed upon by the authors from each session, all statements of agreement were subject to an additional round of voting on the second day of the meeting. Any authors who had to leave the meeting prior to this second round of voting were allowed to submit an absentee vote via email. It is important to note that for 12 of 16 (75%) statements of agreement, a 100% response rate was attained. However, 1 (2.7%) author abstained from voting for statements 9 and 11, and 2 (5.4%) authors abstained from voting for statements 10 and 12, resulting in a response rate of 94.6% to 97.3%. A summary of the final voting results for each statement of agreement is provided in Table 1. Voting results for the Future Directions statements of agreement are presented later in the paper. None of the authors abstained from voting on any of the Future Directions statements of agreement, resulting in a 100% response rate.

Table 1.

Summary of Final Voting Results for each Statement of Agreement.

Key point Disagree Somewhat disagree Somewhat agree Agree Abstain
1. Prior expert consensus for management of concussion included: a) no return to play (RTP) on same day, b) prescribed physical and cognitive rest until asymptomatic, c) accommodations at school/work as needed, and d) progressive aerobic exertion-based RTP based on symptoms. 0 (0%) 0 (0%) 3 (8.1%) 34 (91.9%) 0 (0%)
1. Previous consensus statements have provided limited guidance with regard to the active treatment of concussion. 0 (0%) 0 (0%) 1 (2.7%) 36 (97.3%) 0 (0%)
2. There is limited empirical evidence for the effectiveness of prescribed physical and cognitive rest – with no multi-site RCT for prescribed rest following concussion 0 (0%) 0 (0%) 3 (8.1%) 34 (91.9%) 0 (0%)
3. Prescribed physical and cognitive rest may not be an effective strategy for all patients following concussion. 0 (0%) 1 (2.7%) 8 (21.6%) 28 (75.7%) 0 (0%)
4. Strict brain rest (e.g., stimulus deprivation, “cocoon” therapy) is not indicated and may have detrimental effects on patients following concussion. 0 (0%) 1 (2.7%) 8 (21.6%) 28 (75.7%) 0 (0%)
5. Although most individuals follow a rapid course of recovery over several days to weeks following injury, concussions may involve varying lengths of recovery. 0 (0%) 0 (0%) 0 (0%) 37 (100%) 0 (0%)
6. Recovery from concussion is influenced by modifying factors, the severity of injury, and the type and timing of treatment that is applied. 0 (0%) 0 (0%) 4 (10.8%) 33 (89.2%) 0 (0%)
7. Concussions are characterized by diverse symptoms and impairments in function resulting in different clinical profiles and recovery trajectories. 0 (0%) 0 (0%) 2 (5.4%) 35 (94.6%) 0 (0%)
8. Thorough multi-domain assessment is warranted to properly evaluate the clinical profiles of concussion. 0 (0%) 0 (0%) 0 (0%) 36 (97.3%) 1 (2.7%)
9. A multidisciplinary treatment team offers the most comprehensive approach to treating the clinical profiles associated with concussion. 0 (0%) 0 (0%) 6 (16.2%) 29 (78.4%) 2 (5.4%)
10. Concussion is treatable. 0 (0%) 0 (0%) 2 (6.00%) 34 (91.9%) 1 (2.7%)
11. Preliminary evidence suggests that active rehabilitation may improve symptom recovery more than prescribed rest alone after concussion. 0 (0%) 0 (0%) 7 (18.9%) 28 (75.7%) 2 (5.4%)
12. Active treatment strategies may be initiated early in recovery following concussion. 0 (0%) 0 (0%) 4 (10.8%) 33 (89.2%) 0 (0%)
13. Matching targeted and active treatments to clinical profiles may improve recovery trajectories following concussion. 0 (0%) 0 (0%) 4 (10.8%) 33 (89.2%) 0 (0%)
14. Patients returning to school/work while recovering from concussion benefits from individualized management strategies. 0 (0%) 0 (0%) 7 (18.9%) 30 (81.1%) 0 (0%)
15. Pharmacological therapy may be indicated in selected circumstances to treat certain symptoms and impairments related to concussion. 0 (0%) 0 (0%) 2 (5.5%) 35 (94.5%) 0 (0%)
16. Pharmacological therapy may be indicated in selected circumstances to treat certain symptoms and impairments related to concussion. 0 (0%) 0 (0%) 2 (5.5%) 35 (94.5%) 0 (0%)

SUMMARY OF THE CURRENT APPROACH TO TREATING CONCUSSIONS

  • 1

    Prior expert consensus for management of concussion included: a) no same-day return to play, b) prescribed physical and cognitive rest until asymptomatic, c) accommodations at school/work as needed, and d) progressive aerobic exertion-based RTP based on symptoms.

  • 2

    Previous consensus statements have provided limited guidance with regard to the active treatment of concussion.

Current concussion consensus statements advocate for concussion management strategies including: a) no RTP or activity for individuals with a suspected concussion, b) prescribed cognitive and physical rest until asymptomatic, c) accommodations at school/work as needed, and d) progressive aerobic exertion-based RTP or activity based on symptoms.17,2023 A majority of athletes respond well to this management approach and have a favorable return to full activity. However, some individuals experience persistent symptoms that do not respond to these conventional management strategies.

Most concussion consensus documents have focused on SRC. A summary of statements regarding management of concussion from each of these sport-specific consensus documents is provided in Table 2. Although some of these statements mention that there may be other symptom-based approaches to treating concussion, they provide little in the way of specific, targeted treatment strategies or guidance with respect to the process of active treatment across recovery. The majority of current consensus statements endorse an approach to managing concussion (ie, prescribed rest followed by progressive return to activity) that is dependent on spontaneous resolution of symptoms and impairments, rather than active treatment.17,20,22,23 The most active aspect of previous consensus statements pertains to the use of education strategies and medications, primarily in the sub-acute recovery phase, to help manage specific symptoms (eg, Broglio et al, 201420; Harmon et al, 201323). To date, the focus of consensus documents has not included emerging, active treatment strategies for concussion, resulting in a limited foundation for clinicians treating patients with this injury.

Table 2.

Summary of Recommendations for Management of Concussion in Sport from Current Consensus Documents.

Acute Tx Medications Behavioral Academic Accommodations RTP protocol Other therapies
American Academy of Neurology (2013)21 No same day RTP No evidence based intervention for concussions Cognitive restructuring to prevent PCS Individualized grade plans for cognitive activity Supervised, graded exertion program, asymptomatic off medication -
American Medical Society for Sports Medicine (2013)23 No same day RTP; appropriate disposition to home, ER, etc; frequent awakenings no longer recommended Acetaminophen Relative physical and cognitive rest; in the early stages, athlete should not engage in physical or cognitive activities that result in an increase in symptoms; Dim, quiet environment No standardized guidelines for returning athletes to school; if symptoms develop, athlete may need reduced workload, extended test taking, shortened school day Individualized, gradual, and progressive; normal cognitive/balance evaluation, -
American Academy of Pediatrics (2010)22 No same day RTP; athlete should be monitored for several hours to determine if emergency department is warranted No evidence-based research for medications Discourage activities that require concentration and attention; withhold physical activity until asymptomatic Cognitive rest, including absence from school, shortening school day, reduction of workload, allowance of more time Graded return to play Assessment of mental health problems; Patients with PCS may benefit from exercise training
International Consensus Statement (2013)17 No same day RTP; Physical and cognitive rest until symptoms resolve Treatment for specific symptoms Gradual return to school and social activities, before sport - Graded RTP Low level exercise for those slow to recover; multidisciplinary management for “difficult” patients
National Athletic Trainers’ Association (2014)20 No same day RTP; do not awaken patient unless prolonged LOC/amnesia; no aspirin Over-the-counter, as needed for symptoms Avoid physical activity and limit cognitive activity to not exacerbate concussion symptoms; ADLs that do not exacerbate symptoms may be beneficial and allowed Temporary accommodations should be allowed Should not begin until patient no longer reports symptoms, has normal clinical examination, and normal neurocognitive functioning/motor; Exercise Progression -
National Collegiate Athletic Association (2013)24 No same day RTP; Provide instructions; athletes should not be left alone; avoid alcohol, aspirin; determine if imaging is needed - Physical and cognitive rest until the acute symptoms resolve Some athletes may require academic accommodations, such as reduced workload, extended test-taking time, das off or shortened day Supervised, graded program of exertion Tx for postconcussion syndrome (PCS) and depression is different than tx for acute concussion
Team Physician Consensus Statement-ACSM (2011)25 No same day RTP; determine disposition; communicate with parents/ coaches, etc. - Team physicians should facilitate academic accommodations No medications that mask symptoms; NP testing normal (if performed); progressive aerobic and resistance exercise training -
  • 3

    There is limited empirical evidence for the effectiveness of prescribed physical and cognitive rest – with no multisite RCT for prescribed rest following concussion.

Although the current concussion consensus and position statements suggest patients may benefit from an initial period of physical and cognitive rest,17,20,22,23,26 these recommendations have been formulated primarily from anecdotal evidence, as there have been few high-quality prospective studies conducted regarding the effectiveness of rest. Recommendations for physical rest, which suggest the phased RTP progression does not begin until the patient is asymptomatic or back to baseline symptoms at rest, are included in most RTP guidelines.17,20,22,23,26 Healthcare providers routinely use prescribed physical rest in a variety of clinical settings.27,28 In contrast, healthcare providers prescribe cognitive rest less frequently.29,30 In a survey of pediatric providers, cognitive rest was only included as a written recommendation for 11% of pediatric patients.30 Similarly, researchers reported that cognitive rest was not recommended to any patient seen in the emergency department prior to 2008 and was only recommended to 12% of patients in 2012.29

Evidence for physical and cognitive rest has been characterized in retrospective study designs of small samples of primarily male patients from a single practice15,3134 resulting in equivocal findings. Researchers noted that patients with the highest and lowest levels of activity had worse outcomes31 and took longer to recover,32 suggesting that too much or too little physical and cognitive activity could be detrimental to recovery. In contrast, researchers have reported that a 1-week period of cognitive and physical rest decreased symptoms and increased cognitive scores in nearly 60% of patients even when employed several weeks or months following injury.33 Other researchers have reported no association between prescribed rest and decrease of symptoms34 or recovery time.14 Only 1 small RCT of cognitive and physical rest following concussion has been published.35 These researchers reported that 5 days of strict rest following injury resulted in longer symptom duration and higher number of symptoms compared to usual care recommendations. Collectively, the limited body of evidence appears to be equivocal, however, some studies suggest that that too little30,31 and too much32,34 physical and cognitive rest may delay recovery, whereas an initial brief period of rest may be beneficial. These findings, though preliminary, clearly underscore the need for prospective, multi-site RCTs to inform the use and timing of prescribed rest compared with active treatments following concussion.

  • 4

    Prescribed physical and cognitive rest may not be an effective strategy for all patients following concussion.

The theory underpinning prescribed rest following concussion has been based on 2 tenets: 1) rest decreases exposure to additional head impacts and thus decreases the risk of re-injury during a vulnerable post-injury period,36 and 2) physical and cognitive activity often exacerbate symptoms and associated impairments in the post-injury period, thereby prolonging recovery.37,38 However, it is important to note that avoiding contact during the vulnerable period following concussion and prescribed rest represent 2 separate strategies. As such, avoiding contact during this time is always recommended to avoid further head impacts. In contrast, although prescribed non-contact, sub-acute, physical rest and cognitive rest may exacerbate symptoms, they do not appear to worsen pathophysiological injury or cause additional injury.39 The use of prescribed rest to treat patients with concussion has been based largely on expert consensus opinion,17,20,21 Factors that optimize the effects of prescribed rest (eg, what type, how long, etc.) remain unclear. Anecdotally, athletes with certain symptoms and impairment may tolerate increased early activity, while others may benefit from longer and more complete physical and cognitive rest during the acute post-injury period (see numbers 8, 12, 13). Both early activity and rest approaches may aid recovery and result in favorable outcomes following concussion. However, there is increased concern that too much rest may have negative consequences for patients who are slow to recover.

The deleterious effects of prolonged rest in patients with chronic conditions are well documented in the literature and reported in several chronic conditions ranging from low back pain40,41 to brain injury.42 More than 30 years ago, Relander et al42 randomized adult patients admitted to the hospital from the emergency department with mTBI to bed-rest versus active therapy and reported that subjects in the active therapy group were able to return to work 14 days earlier than the bed-rest group. Relander et al42 concluded that this active treatment was better for patients “who had exaggerated fears about their condition.” More recently, de Kruijk et al43 compared 6 days of bed rest versus no bed rest in a randomized clinical study of bed rest for treatment of concussion and showed no benefit to rest.43 In a retrospective study, Majerske et al31 reported that patients who reported low levels of post-injury physical and cognitive activity in the first month following injury had negative outcomes, whereas patients who reported moderate activity had the best outcomes at follow-up.31 Thomas et al35 randomized adolescents discharged with mTBI to 5 days prescribed physical and cognitive rest versus usual care and found that early, prolonged rest recommendations were associated with delayed recovery and more daily post-concussive symptoms, specifically, more physical symptoms early in recovery and emotional symptoms throughout recovery.35 In this study, researchers also reported that patients diagnosed with mTBI based on post-concussive symptoms alone and patients with a past history of concussion were more likely to have negative outcomes when randomized to 5 days of prescribed physical and cognitive rest. This study informs future research efforts to determine how rest may influence other subgroups of concussed patients. In addition, these data are supported in basic TBI neuroscience studies that document increased blood flow, brain growth factors, and synaptic plasticity following subacute physical (eg, running) and cognitive activity (enriched environment).44,45

The efficacy and utility of prescribed rest is challenged in the literature. Prescribed rest may exert a negative influence through hypervigilance on symptoms, preoccupation with ordered restrictions, reinforcement of negative expectations, social isolation, and removal from patients’ normal routines.4648 For some patients, prescribed physical and cognitive rest may contribute to an increased symptom burden and prolonged recovery and therefore alternative (ie, more active) acute treatment paradigms should be considered.

  • 5

    Strict brain rest (eg, stimulus deprivation, “cocoon” therapy) is not indicated and may have detrimental effects on patients following concussion.

“Cocoon therapy” or “strict brain rest” refers to avoidance of all visual, auditory, light, social, intellectual, or physical exertion/stimulation.49 Although it is generally agreed that most concussed patients benefit from some form of initial physical and cognitive rest, prolonged strict brain rest can lead to social isolation, anxiety, and problems with self-esteem, and potential loss of academic standing in students.50 Additional adverse effects of a strict brain rest protocol include anxiety and depression, “nocebo” effect contributing to the exacerbation of symptoms, physical deconditioning, school delays, and other academic problems related to accumulating work load. Strict brain rest may also result in a cycle of symptoms resulting from prolonged periods of rest due to the self-perpetuation of symptoms in the context of strict brain rest.51 It is also important to note that individualized physical and cognitive activity restriction does not equate to strict brain rest. In conclusion, strict brain rest involving avoidance of nearly all brain stimulation is not empirically supported following concussion and may have unintended adverse effects on patients with this injury.

  • 6

    Although most individuals follow a rapid course of recovery over several days to weeks following injury, concussions may involve varying lengths of recovery.

It has been generally accepted that patients with concussions recover within 7 to 14 days following injury.17,21 However, there is an increasing number of studies that suggest concussion recovery may take longer for some patients and is influenced by demographic modifying factors including age (< 18 years),5254 sex (female),53,55 and history of concussion (>2).53,5659 Furthermore, concussions are heterogeneous, with varying levels of severity as well as injury-related modifying factors (eg, on-field dizziness, post-traumatic migraine) that may affect recovery (see number 7). In short, some patients report symptom recovery within a few days, while others report symptom recovery over a period of months to years.60

Previous research documenting concussion recovery has typically included a homogeneous demographic group, such as male football players, and focused on recovery as measured by symptoms and cognitive performance. As a result, the generalizability of previous findings to the wider community of athletes as well as individuals with non sport-related concussions may be limited. Studies of recovery time following concussion have incorporated varying definitions of recovery including symptom resolution,9,32,34 date of medical clearance (NCAA concussion guidelines), return to baseline performance,53,6165 and statistical recovery.54,66,67 Moreover, there has been considerable variability in the observed length of recovery across studies depending on which criteria or assessment approaches were used to determine recovery. Concussion recovery appears to resolve within 7 days when brief acute assessments of cognition and postural stability are used (eg, Balance Error Scoring System [BESS], Standardized Assessment of Concussion [SAC])64,65,6871 and assessments using symptom reports reveal an interval of recovery from 5 days64,65,69,72,73 to 14 days.7477 Cognitive recovery is even more variable with recovery reported between 764,65,69,70,78 and 21 days.61,75,79 Meta-analytic reviews suggest that neurocognitive deficits persist beyond 14 days across studies.68 However, an earlier meta-analysis supported a 7-day time period for these same deficits.80 On an individual basis, factors including litigation, worker’s compensation, and the population affected (eg, sport, military, civilian) may influence differences in these and other concussion-related outcomes. Recently, researchers have reported that when using comprehensive assessment approaches that include symptoms, cognitive, and vestibular-oculomotor reports, concussion recovery may extend up to 21–28 days in high school and college-aged athletes.66 The findings from this study also indicate that concussion recovery may be domain-specific (ie, cognitive recovery persists longer than self-reported symptoms and vestibular/oculomotor assessment) and are influenced by certain modifying factors such as sex (ie, females demonstrate a longer recovery). Although the majority of studies utilize common clinical tools that assess a variety of domains to determine recovery, recent neuroimaging studies report persistent findings in concussed patients that may reflect even longer recovery times.8183 In summary, these findings suggest that recovery following concussion may vary considerably depending on the variables used to identify recovery and the populations that are being examined.

  • 7

    Recovery from concussion is influenced by modifying factors, the severity of injury, and the type and timing of treatment that is applied.

Consensus statements17,2023,84 and researchers suggest that demographic and injury-related modifying factors, and the type and timing of certain treatments can influence concussion recovery.14,51,85 The frequency, severity, and recovery from concussion are influenced by demographic (eg, age (< 18 years old),53,54 sex (female),53,8688 concussion history,58,8993 and premorbid factors including migraine,94 depression,95 anxiety,96 learning disability,78 hyperactivity disorders,97 sleep disturbance,55,98 and overall symptom burden.99 In addition, factors related to symptom severity have been associated with prolonged recovery including post-traumatic amnesia (PTA),9,100 loss of consciousness (LOC),101 on-field dizziness,102 post-traumatic migraine,11,103,104 acute symptom burden,69,77,105,106 and neurocognitive impairment.75,76 The severity of biomechanical forces and/or trauma is associated with prolonged recovery in mTBI patients in both civilian84 and military107 populations, however this relationship in sport and recreation populations is tenuous due to a limited number of studies and the difficulty in reliably connecting biomechanical impacts to concussion diagnosis and recovery outcomes.108112 The type and timing of concussion treatments (eg, educational, behavioral, ocular-motor, vestibular, physical, and pharmacological) may expedite recovery,85,113 however if not executed properly, may unintentionally prolong recovery.14,31,35 For example, prescribed cognitive and physical rest is recommended in consensus statements as the initial treatment approach for concussion17,2023 however these statements provide very little guidance on the timing and type of rest.

In summary, concussions are highly individualized injuries due in part to the effects of modifying factors, the severity of the injury, the type and timing of treatment, socio-cultural factors, and the clinical symptoms and diverse functional impairments exhibited by the patient. Clinicians should consider these factors when evaluating concussions, educating the patient, family, teachers and employers, and devising and implementing an active treatment approach to concussion care.

Heterogeneity and Evolving Clinical Profiles of Concussion

  • 8

    Concussions are characterized by diverse symptoms and impairments in function resulting in different clinical profiles and recovery trajectories.

As discussed in previous sections, concussions are heterogeneous and characterized by varied symptom presentation, which calls into question the general recommendation that all concussion patients be prescribed physical and cognitive rest until they are asymptomatic. Recently, clinical researchers have attempted to characterize or classify concussion into specific clinical profiles.114,115 Collins and colleagues114 categorized concussions into 6 clinical profiles including: 1) vestibular, 2) ocular-motor, 3) cognitive/fatigue, 4) post-traumatic migraine, 5) cervical, and 6) anxiety/mood. These clinical profiles can be applied in the first week following injury, are not mutually exclusive, and may overlap and involve primary, secondary, and tertiary profiles. Each concussion profile carries specific evaluation and treatment/rehabilitation recommendations. Ellis and colleagues115 proposed a conceptual framework with 3 main post-concussion disorders, 1) physiological, 2) vestibulo-ocular, and 3) cervicogenic. In addition, these researchers describe 2 post-concussion modifying factors: post-traumatic mood disorders and migraine. In this model, a period of 3 weeks is required before patients can be categorized and the determination requires evaluation of the patient’s clinical history and the physical and symptom-based response to exercise treadmill testing. Potential overlap among the 3 main concussion profiles is not discussed.115

Both models provide direction for treatment based on a heterogeneous injury classification system. The adoption of concussion profiles may align the management of SRCs with that of non-sport concussions. For example, guidelines from civilian and military mTBI have begun to address the heterogeneous nature of concussion. In 2009 the Veterans Administration and the Department of Defense recommended evaluation and individualized treatment based on the presentation of certain symptoms including post-traumatic headache, insomnia, cognitive dysfunction, and mood-related symptoms in service members with persistent symptoms beyond 7 days.116 In 2011 the Ontario Neurotrauma Foundation and the Canadian MTBI Consensus group both recommended a targeted evaluation and treatment of post-traumatic headache, insomnia, cognition, mood, balance, vision, and fatigue but only for those with symptoms persisting more than 3 months.117,118 The pediatric version of the ONF guidelines published in 2014 also included a targeted, subject-specific evaluation for patients with symptoms lasting more than 1 month.119

The identification of clinical profiles may prove useful by emphasizing the need for multidimensional assessment and developing treatment approaches that are targeted to symptom presentation and findings from clinical evaluation. However, care must be exercised to not minimize individualized approaches by attempting to place patients into rigid profiles as profiles often overlap. The use of clinical profiles to characterize symptoms and impairment provides the framework for targeted treatments to match specific concussion profiles and recovery trajectories. It is important to note that although clinical profiles are both intuitive and supported anecdotally, to date they have not been empirically validated. As such, more research and clinical evidence are required to examine current and emerging concussion clinical profiles to further refine this targeted, active treatment approach.

  • 9

    Thorough multi-domain assessment is warranted to properly evaluate the clinical profiles of concussion.

Concussion is a complex, heterogeneous injury that presents with a variety of functional deficits and clinical findings, which warrant a thorough evaluation to appropriately assess the injury and treat the injury. Both the acute assessment of a potential concussion and subsequent evaluations should involve a systematic, careful examination. The primary goal of the acute evaluation is to determine whether a concussion has occurred and implement immediate steps for care. The goals of the sub-acute evaluation are to characterize the clinical presentation and profiles of the injury, including multi-domain levels of functioning, and prescribe an individualized treatment plan.17,21,23,114,115,120

Although clinical presentations are highly variable, certain clinical profiles are often identifiable via the use of a multi-domain assessment, which may include:

  • Review of mechanism of injury, specifically location, force, and direction of trauma17,21,23,114,115,120

  • Relevant past medical history including age, gender, prior concussion history, and comorbid “concussion risk factors”77,95,102,121

  • Symptom identification using symptom checklists17,21,23,114,115,120

  • Neurocognitive screening or neuropsychological evaluation61,75,76,93,102,122126

  • Balance assessment58,123,127,128

  • Vestibular screening or examination85,115,129

  • Assessment or screening of ocular motor function115,129131

  • Neurological exam17,21,23,114,115,120

  • Examination of the cervical spine114,120,132

  • Consideration of neuroimaging if indicated133135

  • Evaluation of psychological factors associated with concussion17,136,137

It is important to recognize that the list above is not exhaustive and each of the above components represent 1 aspect of a comprehensive concussion evaluation approach and should not be used in a stand-alone manner. Taken together, the evaluation of each of these components provides a thorough, multi-domain assessment. This approach allows clinicians to better define the injury, thereby providing appropriate direction and education regarding recovery expectations, rehabilitation measures, treatment options, and potential prescriptive therapeutic interventions.

  • 10

    A multidisciplinary treatment team offers the most comprehensive approach to treating the clinical profiles associated with concussion.

The heterogeneous presentation and clinical profiles of concussion may require access to an array of healthcare specialists from multiple disciplines to help design and execute targeted treatment plans, and educate individuals and their families. The formation of multidisciplinary approaches to concussion care and healthcare provider networks may result in improved standardization of care, decreased resource utilization, and better ensure the provision of services for concussion.138140 At the core of the multidisciplinary team is the coordinating healthcare provider, typically a physician (ie, neurologist, neurosurgeon, primary care/sports medicine physician, emergency medicine physician, physical medicine and rehabilitation physician) or clinical neuropsychologist.139 In addition, other healthcare specialties may be involved in specific aspects of the care for patients with concussion including the physical or vestibular therapist, athletic trainer, optometrist or ophthalmologist, speech and language pathologist, clinical or sport psychology professional, or occupational therapist). Lastly, it is important to note that the creation of multi-disciplinary teams may vary based on the resources locally available. For example, in rural areas individuals from multiple specialties may not be readily accessible, which may necessitate the development of consultative relationships and emerging technologies including telehealth.

Targeted Evaluation and Active Management Approach to Concussion: Specific Strategies

  • 11

    Concussion is treatable.

Although there are no recognized treatments for the underlying pathophysiology of concussion, there is agreement among experts that the clinical spectrum of concussion symptoms and impairments are treatable.141 There is already published empirical evidence that concussion is treatable through active approaches involving earlier activity,35 aerobic exertion,142 vestibular,85,132 and vision143 therapies. Overall, these studies demonstrate that active treatments are more effective than rest-based approaches.

A major focus of current clinical efforts that involves associating a comprehensive examination of the symptoms, impairments, and clinical profiles of concussion may lead to the identification of targeted treatment pathways that may expedite recovery.16,114,138 The treatment of concussion symptoms and impairments is evolving. Past practice of prolonged rest (see DiFazio et al, 2016)50 has advanced to current hypotheses on the benefits of more active approaches to rehabilitation including vestibular,132,144 oculomotor/vision,143,145 and behavioral146 therapies. Active rehabilitation involves an interdisciplinary approach directed at addressing and treating the specific, individual symptoms, impairments, and clinical profiles that may be identified at clinical presentation.

The role of active rehabilitation and treatment strategies in changing the underlying concussion pathophysiology and concomitant recovery process in the brain needs further study. A detailed history and clinical examination together with a multidimensional assessment of patients with concussion may help identify distinct clinical profiles that can guide treatment and potentially improve the trajectory of recovery (see number 9).114,138 As with other diseases and injuries, there are many treatments that are directed at alleviating the signs and symptoms while the underlying disease or injury process runs its course (eg, common cold, minor sprains). However, those same treatments may not alter/treat the underlying disease or injury process. Similarly, treatments for concussion are directed at symptoms and impairments and are vital to current individualized concussion management.

The current consensus is that evidence-based treatments for the underlying pathophysiology of concussion are lacking. Moreover, until more data are available, healthcare providers should be mindful of over-utilizing or advertising unproven treatments that lack empirical support and validation, and that may lead to complications. Additional evidence-based research is needed to better determine the mechanism and effectiveness of targeted active interventions on the underlying pathophysiology of concussion. Nonetheless, emerging evidence indicates that active treatment of concussion is effective for some patients.

  • 12

    Preliminary evidence suggests that active rehabilitation may improve symptom recovery more than prescribed rest alone after concussion.

  • 13

    Active treatment strategies may be initiated early in recovery following concussion.

Active treatment with a patient can be initiated on the day of the injury. Three studies provide evidence for the effectiveness of concussion education in the Emergency Department on managing injury expectations in adults147 and children.148,149 Patients and families who received explicit discharge education and management strategies related to their symptoms exhibited more positive recovery outcomes than control participants. There is limited empirical evidence for the presumed relationship of prescribed physical and cognitive rest to a subsequent decrease in symptoms and cognitive impairment.33 As such, more active approaches to treating concussion may be effective for certain patients (see number 4). Findings from animal studies demonstrate that an “enriched environment” of physical and cognitive stimulation enhances histologic, cognitive, and behavioral recovery from TBI.150152 An enriched environment consists of opportunities to participate in physical activities, social networks, and intellectual activities, most of which are restricted when rest is prescribed for patients. In contrast, impoverished environments, particularly during brain maturation, are reported to stunt synaptic plasticity and cognitive development.153,154

Emerging empirical research suggests that exposing patients with persistent post-concussive injury to supervised low level physical activity is not only safe153 but effective.13,31,155159 Brief submaximal (60% submaximal capacity) aerobic training, sport-specific light coordination activity, vestibular therapy, treadmill exercise, visualization, and home exercises have been utilized safely as exertional activity in patents with persistent concussion symptoms.155157 The report of the Institute of Medicine of the National Academies on concussion in sport stated, “there is little evidence regarding the efficacy of rest following concussion or to inform the best timing and approach for return to activity…” and recommended RCTs to determine the efficacy of physical/cognitive rest.160 Although the specifics of timing and exertion type have yet to be determined empirically, it is the agreed opinion of the authors that preliminary clinical evidence suggests that supervised individually tailored active physical and cognitive rehabilitation may improve symptom recovery more than prescribed rest alone after concussion, and that active treatment strategies may be initiated early during recovery from concussion. Regardless of this opinion, additional RCTs are warranted to compare the benefits of prescribed physical rest to more physically active (ie, physical exertion) treatments.

  • 14

    Matching targeted and active treatments to clinical profiles may improve recovery trajectories following concussion.

Although there are no clear evidence-based treatments for concussion, emerging clinical research and observations suggest that recovery after concussion may be facilitated when targeted, active interventions are matched to the patient’s clinical profile based on presentation and history.16,114,115,138 For example, patients that present with post-concussion vestibular impairment and symptoms (eg, dizziness, vertigo, impaired balance, visual motion sensitivity) may benefit from vestibular rehabilitation exercises that treat benign paroxysmal positional vertigo (BPPV) and improve balance, gaze stability, eye-head coordination and gait.144 Similarly, the efficacy of vision therapy was recently reported to be beneficial for patients with concussion and mild TBI that exhibited common oculomotor issues such as reading difficulty, vergence, accommodation, saccade, or pursuit impairment.143,145 Vision therapy (orthoptics), employs a variety of vision exercises and tools designed to improve oculomotor control, focusing, coordination, and teaming. In addition to vestibular rehabilitation and vision therapy, exercise prescribed as an adjunct to other therapies or medication may reduce symptoms of depression and anxiety,161,162 and may prevent or modify the intensity of migraines that often accompany concussion.11,103,163165 As another example, patients who are slow to recover after concussion may benefit from the addition of exertion training programs.155,156,166 Patients experiencing psychological and behavioral effects following concussion such as anxiety96,167 and depression11,167,169 may benefit from cognitive behavioral therapy (CBT) and other psychotherapeutic and behavioral interventions.121 Finally, cervical dysfunction and cervicogenic headaches occurring after concussion may be managed with manual therapy to the cervical spine and head/neck proprioceptive re-training.115,132

No single treatment strategy will be effective for all patients following concussion due to the individualized nature of the injury and its clinical consequences. Multiple active rehabilitation strategies are now available with growing evidentiary basis for efficacy when matched to specific symptoms and impairments.

  • 15

    Patients returning to school/work while recovering from concussion benefit from individualized management strategies

Following concussion, the active return to school and work is a major priority for the recovering patient.26 Appropriate individualized supports must be in place to facilitate recovery for the symptomatic student/employee.170 To support this return, symptom and clinical profile-targeted accommodative supports and adjustments may be necessary to balance the goals of recovery and return to productivity. For example, in patients with vestibular dysfunction, modifications in the school environment to lessen the triggers for their symptoms, such as removal from gym or dance class, band/orchestra, or school assemblies may be employed. Injured students with oculomotor dysfunction may require delaying their tests/quizzes and reducing the amount of homework during the initial recovery period. Support should be individualized based on clinical presentation, symptoms and impairment, patient history, and assessment results. It is important to support the recovering student, but also ensure that modifications are not prolonged when no longer necessary or do not provide an unfair advantage to the injured student. These issues can be determined by serial multi-domain assessment and monitoring of the patient’s status.

Presently, no multisite clinical trials have been conducted to validate which specific treatments, their timing or duration will facilitate successful return to school and work. Although clinical recommendations provide clinicians and school personnel with practical and logical suggestions, their application requires further research to demonstrate optimal benefit and avoid excessive or unnecessary use. The underlying premise to these interventions is that active, progressive school-based management with concussion clinical profile-targeted recommendations may mitigate adverse effects on school learning and work productivity, reduce patient concerns on the impact of the injury on performance, and lower the risk of prolonged recovery. In the school context, Gioia advocates for explicit training of medical and school systems to facilitate the student’s individualized program of gradual return, identifying key symptom targets tied to accommodation strategies, monitoring progress, and applying systematic criteria for progression to the next less restrictive level of support.170 Prolonged absence from one’s school or work environment must be avoided to reduce the risk of secondary adverse social and emotional effects (eg, anxiety) from disengagement and lack of involvement in previously enjoyed activities. To inform treatment-relevant targets, Ransom et al171 provide initial evidence for the impact of concussion on academic learning and performance (eg, headaches and fatigue interfering with learning, greater difficulty understanding new material).

Several clinically-based support systems are available to guide symptom-targeted school interventions including the CDC’s “Heads Up to Schools: Know Your Concussion ABC’s”;172 Colorado’s Remove/Reduce, Educate, Adjust/Accommodate, Pace (REAP) program;173 BrainSTEPS;174 and The Brain 101 Schoolwide Concussion Management program.146 The Brain 101 program was first implemented through a randomized controlled trial. The program incorporates skills training, guidelines on creating a concussion management team, and symptom-targeted strategies for supporting students in the classroom. Students in the Brain 101 intervention group received more individualized/customized academic accommodations than students in control schools. This study demonstrated significant increases in sports concussion knowledge, knowledge of academic management strategies, and plans to implement these concussion management strategies.146 Additional evidence from a multisite pediatric concussion education program in the Emergency Department demonstrated that early education via focused concussion discharge instructions and a Return to School letter increased implementation of academic supports at school.149 Evidence-based systematic protocols for return to work following concussion do not currently exist, although clinical recommendations for returning employees are provided on the ACE Care Plan-Work version in the CDC Heads Up to Healthcare Providers175 including schedule considerations (eg, shortened work day, more frequent breaks) and safety considerations (eg, not lifting heavy loads, operating risky machinery). Continued investigation of effective, targeted interventions based on symptoms and impairment for return to school and work via multi-site RCTs is warranted.

  • 16

    Pharmacological therapy may be indicated in selected circumstances to treat certain symptoms and impairments related to concussion.

There is little randomized-controlled data on the effectiveness of pharmacological therapies in patients with concussion. Nonetheless, in the collective clinical experience of the authors with a wide variety of concussion patients over many years, optimal treatment can be obtained using a combination of 3 elements: a) active treatment and rehabilitation, b) lifestyle management, and c) pharmacological therapies; Pharmacological therapies should target specific symptoms and impairments. For example, cognitive deficits might be treated using direct or indirect stimulants, whereas, migraine symptoms might be treated using triptans. We should note that a blanket approach to treating all patients with a concussion using the same pharmacological therapy is contraindicated and should be avoided. Although there is limited empirical evidence for pharmacological therapies (eg, for amantadine113), many of these approaches are discussed in recent reviews6,16 and concussion care guides. We encourage the reader to review these guides for more specific recommendations regarding pharmacological therapies. The timing of pharmacological therapies may be influenced by pre-existing conditions. For example, a patient with a history consistent with migraine headaches may benefit from earlier administration of a migraine prophylactic medication. Similarly, a patient with a history consistent with depression may benefit from earlier administration of an antidepressant. Additionally, patients already on such medications may benefit from a temporary increase in their medication. Conversely, decreasing or discontinuing a patient’s medication in the setting of concussion may exacerbate symptoms. However, it is also important to avoid certain pharmacological therapies that can, based on our collective clinical experience, worsen overall recovery following concussion. In general, it is recommended that clinicians avoid the following: 1) routine-defined as more than 3 days per week for 2 weeks or more-use of narcotics, butalbital preparations, and pain medication; 2) neuroleptics, excess alcohol, benzodiazepines, and anticholinergics such as diphenhydramine as routine treatments for insomnia; 3) leviteracetam in patients with mood instability; and 4) sedating medications in patients with severe fatigue and hypersomnia. In conclusion, collective clinical experience indicates that judicious pharmacological therapies can in many cases provide symptomatic benefit following concussion. However, the lack of empirical data to support specific prescription guidelines for the use of pharmacological therapies for patients, concussion highlights the need for additional research in this area.

Future Directions: A Call to Research

An important objective of this paper and the preceding meeting was to provide suggestions for researchers and clinicians to consider as next steps to build on the statements of agreement above. To that end, the future directions statements of agreement in Table 3 were developed and supported. We also believe that in order to capitalize on the momentum of this paper sport, military, and public health organizations should act on the future directions in Table 3 by directing funding to expand our understanding of the symptoms and impairments for concussion clinical profiles, biomarkers to assess injury and recovery, and the effectiveness of targeted, active treatments. It is important to note that although it was outside of the scope of the current paper and meeting, we believe that there is a need for further research on biomarkers (eg, neuroimaging, blood) to assess concussion and the effectiveness of any proposed treatments.

Table 3.

Summary of Final Voting Results for Future Directions Statements of Agreement.

Future Directions Disagree Somewhat disagree Somewhat agree Agree Abstain
1. There is growing empirical support for the heterogeneity of this injury and clinical subtypes, but additional research in these areas is warranted. 1 (2.7%) 2 (5.4%) 4 (10.8%) 30 (81.1%) 0 (0%)
2. The clinical benefits (eg, more rapid recovery time, more complete restoration of function, reduced risk of repeat injury, etc) of prescribed active interventions require further study, ideally through RCT’s. 0 (0%) 0 (0%) 5 (13.5%) 32 (86.5%) 0 (0%)
3. Complementary and integrative therapies for concussion require additional research. 0 (0%) 2 (5.4%) 8 (21.6%) 27 (74.0%) 0 (0%)
4. The role of modifying factors on the effectiveness of treatments warrants further investigation. 0 (0%) 0 (0%) 6 (16.2%) 31 (83.8%) 0 (0%)
5. Little is known about the effectiveness of early (ie, acute, sub-acute) interventions and treatments for patients with concussion. 2 (5.4%) 11 (29.7%) 11 (29.7%) 13 (35.1%) 0 (0%)
6. Multi-site, prospective studies of concussion treatments across various post-injury time points are needed. 0 (0%) 0 (0%) 2 (5.4%) 35 (94.6%) 0 (0%)
7. There is a need and a role for empirically- and clinically-based treatment and rehabilitation approaches, as we await validation through prospective studies. 0 (0%) 0 (0%) 7 (18.9%) 30 (81.1%) 0 (0%)

CONCLUSION

Recent evidence challenges the prevailing notion that management of concussion should be based primarily on prescribed cognitive and physical rest. Furthermore, a uniform approach involving prescribed rest may not be effective for all patients; strict brain rest is contraindicated and may exacerbate the effects of this injury. Surprisingly, there has been limited focus in the literature and previous consensus meetings on active approaches to treating concussion. Concussions are characterized by diverse symptoms and impairments and recovery from this injury may vary depending on modifying factors, injury severity, and treatments. Emerging concussion clinical profiles determined via a comprehensive multi-domain assessment may help inform more targeted approaches to treating this injury. Concussion symptoms and impairments are treatable and active rehabilitations involving a multidisciplinary treatment team may enhance recovery. Matching treatments to specific symptoms, impairments, and clinical profiles may also improve recovery following concussion. Return to school/work following concussion presents a unique challenge to clinicians that can be enhanced using an individualized approach. In certain instances, the judicious application of pharmacotherapies may be effective for patients with certain clinical profiles. Additional research is needed to validate concussion clinical profiles, identify biomarkers to assess the effectiveness of treatments, and determine the best timing of specific concussion treatments.

EXECUTIVE SUMMARY.

Purpose of the Statement

  • To challenge common misconceptions about treating concussion.

  • To review the current state of treatment for concussion.

  • To describe and discuss interdisciplinary, targeted evaluation and active management approaches for treating concussion.

  • To describe empirical gaps in existing research related to the treatment and rehabilitation of concussion.

  • To identify areas requiring further research.

Importance of the Statement

  • Many clinicians and the public do not recognize that concussions are a treatable injury.

  • Evidence-based guidance on effective treatments for concussion is lacking, making it difficult for clinicians to determine how best to treat patients with this injury.

  • Clinicians from a variety of healthcare disciplines and with various degrees and backgrounds commonly treat patients with concussions.

  • Conventional treatment for concussion focuses on an approach involving prescribed rest and progressive return to activity.

  • In spite of general perceptions to the contrary, although exertion may occasionally exacerbate symptoms following concussion, it is unlikely to cause additional brain damage/injury.

  • Concussions are individualized injuries characterized by diverse and variable physical, cognitive, emotional, and sleep-related symptoms and impairment.

  • Patient-centered treatments for concussion involving active approaches may benefit recovery for certain patients.

  • This statement may be useful in guiding the treatment of concussions that result from sport and recreational activities, motor vehicle collisions, falls, assaults, and those occurring during military service.

KEY POINTS OF AGREEMENT.

Summary of the Current Approach to Treating Concussion

  • 1

    Prior expert consensus for management of concussion included: a) no same-day return to play (RTP), b) prescribed physical and cognitive rest until asymptomatic, c) accommodations at school/work as needed, and d) progressive aerobic exertion-based RTP based on symptoms.

  • 2

    Previous consensus statements have provided limited guidance with regard to the active treatment of concussion.

  • 3

    There is limited empirical evidence for the effectiveness of prescribed physical and cognitive rest, and no multi-site randomized controlled trial (RCT) for prescribed rest following concussion.

  • 4

    Prescribed physical and cognitive rest may not be an effective strategy for all patients following concussion.

  • 5

    Strict brain rest (eg, stimulus deprivation, “cocoon” therapy) is not indicated and may have detrimental effects on patients following concussion.

  • 6

    Although most individuals follow a rapid course of recovery over several days to weeks following injury, concussions may involve varying lengths of recovery.

  • 7

    Recovery from concussion is influenced by modifying factors, the severity of injury, and the type and timing of treatment that is applied.

Heterogeneity and Evolving Clinical Profiles of Concussion

  • 8

    Concussions are characterized by diverse symptoms and impairments in function resulting in different clinical profiles and recovery trajectories.

  • 9

    Thorough multi-domain assessment is warranted to properly evaluate the clinical profiles of concussion.

  • 10

    A multidisciplinary treatment team offers the most comprehensive approach to treating the clinical profiles associated with concussion.

Targeted Evaluation and Active Management Approach to Concussion: Specific Strategies

  • 11

    Concussion is treatable.

  • 12

    Preliminary evidence suggests that active rehabilitation may improve symptom recovery more than prescribed rest alone after concussion.

  • 13

    Active treatment strategies may be initiated early in recovery following concussion.

  • 14

    Matching targeted and active treatments to clinical profiles may improve recovery trajectories following concussion.

  • 15

    Patients returning to school/work while recovering from concussion benefit from individualized management strategies.

  • 16

    Pharmacological therapy may be indicated in selected circumstances to treat certain symptoms and impairments related to concussion.

Future Directions: A Call to Research

  • There is growing empirical support for the heterogeneity of this injury and clinical profiles but additional research in these areas is warranted.

  • The clinical benefits (eg, more rapid recovery time, more complete restoration of function, reduced risk of repeat injury, etc.) of prescribed active interventions require further study, ideally through RCTs.

  • Complementary and integrative therapies for concussion require additional research.

  • The role of modifying factors on the effectiveness of treatments warrants further investigation.

  • Multisite, prospective studies of concussion treatments across various post-injury time points are needed.

  • There is a need and a role for empirically- and clinically-based treatment and rehabilitation approaches, as we await validation through prospective studies.

  • There is a need for further research on biomarkers (eg, neuroimaging, blood) to assess concussion and the effectiveness of any proposed treatments.

Acknowledgments

Funding: The TEAM Approaches to Treating Concussion Meeting was supported by grants from the National Football League and UPMC

The authors would like to acknowledge the following individuals who were participating investigators who attended the meeting, assisted in the development of the statements of agreement, and provided feedback on the manuscript:

Debra Babcock, MD, PhD (NIH, Washington, DC), Jeneita Bell, MD (DCD, Atlanta, GA), George Chiampas, DO (US Soccer, Chicago, IL), Peter Chiarelli, Gen (Ret.) (One Mind, Seattle, WA), Joan Demetriades (One Mind, Seattle, WA), Dallas Hack, MD, Col (Ret.) (Brain Health Consultant; NCAA, Indianapolis, IN), Brian Hainline, MD (NCAA, Indianapolis, IN)), Col. Sidney R. Hinds II, MD (Defense and Veterans Brain Injury Center, Silver Spring, MD), Hamish Kerr, MD (USA Rugby, Albany, NY), Patrick Kersey, MD (USA Football, Indianapolis, IN), Jennifer Langton (NFL, New York, NY), Mark Lovell, PhD (ImPACT Applications, Inc., Pittsburgh, PA), Jeff Miller, JD (NFL, New York, NY), Kelly Ryder, DC (The Ryder Clinic, Dallas, TX), Richard Shoge, PhD (US Army Medical Research and Material Command at Ft. Detrick, MD), Capt Jeffrey Timby, MD (US Marine Corps Health Services Headquarters, Arlington, VA).

The authors would like to thank the following individuals from Department of Orthopaedic Surgery, UPMC Sports Medicine Concussion Program, University of Pittsburgh, Pittsburgh, Pennsylvania for their contributions to the meeting and the paper: Jamie McAllister-Deitrick, PhD, Alicia Sufrinko, PhD, Melissa N. Womble, PhD, Valerie Reeves, PhD, Cyndi Holland, MPH.

Abbreviations

ARS

audience response system

RCT

randomized controlled trial

SRC

sport and recreation related concussion

RTP

return to play

Disclosure

Dr Collins is a developer and shareholder in ImPACT Application Inc. He receives research funding from the Department of Defense, NCAA, NIH, and GE-NFL. Dr Okonkwo receives research funding from the NIH, Department of Defense, and GE-NFL. He is a paid consultant for Lanx. Mr Almquist receives an honorarium for presentations from ImPACT Applications, Inc., is owner of JLA Consulting, LLC, and co-developer of BrainTrax. Dr Barisa is on the ImPACT speakers’ bureau. Dr Bazarian receives grant/research support from Banyan Biomarkers and Brainscope, is a consultant for Banyan Biomarkers, a virtual shares stockholder in Black Biometrics, and is on the data safety and monitoring board for Neuren Pharmaceuticals. Dr Brody receives grant/research support from Health South and Pfizer, is a consultant for Pfizer Inc., Intellectual Ventures, Signum Nutralogix, Kypha Inc., Sage Therapeutics, iPerian Inc., and Avid Radiopharmaceuticals (Eli Lily & Co.). Dr Cantu serves as Vice Presigent for the National Operating Committee on Standards for Athletic Equipment (NOCSAE), is Co-Founder, Chairman, and Medical Director for Sports Legacy (SLI, Waltham, MA), is Senior Advisor to the NFL’s Head, Neck and Spine Committee, providing expert witness testimony in trials. Dr Cardenas has an Arizona Super Bowl Host Committee grant for a domestic violence program, is a consultant in the NFL unaffiliated neurotrauma consultant program, and serves on the ImPACT application scientific advisory board. Dr Clugston receives grant/research support from Banyan Biomarkers, Inc., and the NCAA-DoD CARE Consortium. Dr Elbin receives grant/research support from Brainscope Company, Inc. Dr Ellenbogen receives grant/research support from NIH and MCI, is an unpaid consultant for NFL-GE and a member of the NFL Head, Neck, and Spine Committee, and is a scientific consultant for the VICIS Helmet Company. Mrs Fonseca is a consultant for ImPACT Applications, Inc. Dr Gioia is a test author for Psychological Assessment Resources, Inc., and a consultant for the Washington Capitals and Baltimore Ravens. Dr Heyer is a consultant for the Carolina Panthers and is President of the NFL Physicians Society. Dr Hotz receives grant/research support from GE-NFL. Dr Iverson receives grant/research support from several organizations for mTBI. He is a salaried as an independent practitioner in neuropsychology, including giving expert testimony, for NeuroHealth Research and Rehabilitation, Inc., NeuroHealth LLC. He receives reimbursements from government, professional scientific bodies, and commercial organizations for discussing/presenting mTBI. Dr Manley receives grant/research support from NIH, DoD, and Abbott. Dr Maroon is employed by the University of Pittsburgh Medical Center which has received grants from the National Football League and the Pittsburgh Steelers. He is an unpaid consultant for the Pittsburgh Steelers football club. He has been the team neurosurgeon for the Pittsburgh Steelers since 1981 and the medical director for World Wrestling Entertainment Corporation since 2008 for the management of spine and brain-related injury. He also has served on the National Football League’s Head, Neck and Spine Committee since 2007 and is currently a consultant to the committee. He is a founder and shareholder in ImPACT (Immediate Post Concussion Assessment and Cognitive Testing), and the WWE has partnered with ImPACT to provide concussion management. He has served as an expert witness in medical legal cases involving concussions. Dr McCrea receives grant/research support from GE-NFL Head Health Challenge I. He is a GE Healthcare consultant and a member of the NFL Head, Neck and Spine Committee. Dr Mucha has received speaker’s fees/honoraria from CE Speakers’ Bureau-American Physical Therapy Association, Medbridge Education, ImPACT Applications, Inc., Brainsteps, Inova and various healthcare and/or educational societies. Dr Podell receives grant/research support from GE-NFL Head Initiative and Brainscope. Dr Shetty receives grant/research support from GE-NFL, Chembio, and Abbott and is on the GE-NFL Medical Advisory Board. Dr Solomon receives DoD grant/research support, is a consultant for University of Tennessee Athletics, TN Tech Athletics, the Tennessee Titans, and Nashville Predators, and is on the Advisory Board of ImPACT Applications, Inc. He has received speaking honoraria from the American Academy of Neurology, American Medical Society for Sports Medicine, and American Associations of Neurological Surgeons. Dr Zafonte receives grant/research support from NIH, DoD, NIDILRR, and NFLPA and is a consultant for Harvard Football. He has relationships with Oakstone Publishing, Demos Publishing, Oxeia Biopharma, and Myomo Orthotic Devices.

The following authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. Dr Kontos receives research funding from the NIH, NCAA, Department of Defense, and GE-NFL. Dr Bailes is Chairman for the Pop Warner Football medical advisory board. Dr Bloom is a consultant for the Carolina Hurricanes. Dr Echemendia is a consultant to the NHL, Major League Soccer, the US Soccer Federation, and Princeton University. He is PI or co-PI on grants funded by NOCSAE, AMSSM, and the New Jersey Commission on Brain Injury Research. Dr Guskiewicz is a member of the NCAA Health and Safety Advisory Committee for Concussion, a member of the NFL Head, Neck and Spine Committee, has given paid expert testimonials for TBI cases, and receives research funding from NIH, NCAA, NFL, USA Hockey, and NATA. Dr Jordan is a paid consultant for NFL Benefits Association for Neurocognitive Disability Benefit. He receives compensation from Innovative CEUs for coaching their education program and is Chief Medical Officer of the NY State Athletic Association. Dr McAllister receives research funding from the NCAA-DoD. Dr Pieroth is a consultant for the Chicago Bears, Whitesox, and Blackhawks. Dr Sills is on the Medical Board of the Federation Equestrian Internationale, is an unpaid consultant for the US Equestrian Foundation, Southeastern Conference and the Nashville Predators, and is an unaffiliated neurotrauma consultant for the NFL. Dr Yates is the team physician for the Pittsburgh Steelers and a member of the NFL Head, Neck and Spine Committee. Drs Cohen, Pombo, Thomas, and Valovich have no funding to disclose.

References

  • 1.Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil. 2006;21:375–378. doi: 10.1097/00001199-200609000-00001. [DOI] [PubMed] [Google Scholar]
  • 2.Bakhos LL, Lockhart GR, Myers R, Linakis JG. Emergency department visits for concussion in young child athletes. Pediatrics. 2010;126:e550–e556. doi: 10.1542/peds.2009-3101. [DOI] [PubMed] [Google Scholar]
  • 3.Rosenthal JA, Foraker RE, Collins CL, Comstock RD. National High School Athlete Concussion Rates From 2005–2006 to 2011–2012. Am J Sports Med. 2014;42:1710–1715. doi: 10.1177/0363546514530091. [DOI] [PubMed] [Google Scholar]
  • 4.Kurowski B, Pomerantz WJ, Schaiper C, Gittelman MA. Factors that influence concussion knowledge and self-reported attitudes in high school athletes. J Trauma Acute Care Surg. 2014;77:S12–17. doi: 10.1097/TA.0000000000000316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Baillargeon A, Lassonde M, Leclerc S, Ellemberg D. Neuropsychological and neurophysiological assessment of sport concussion in children, adolescents and adults. Brain Inj. 2012;26:211–220. doi: 10.3109/02699052.2012.654590. [DOI] [PubMed] [Google Scholar]
  • 6.Elbin R, Covassin T, Gallion C, Kontos AP. Factors Influencing Risk and Recovery from Sport-Related Concussion: Reviewing the Evidence. SIG 2 Perspectives on Neurophysiology and Neurogenic Speech and Language Disorders. 2015;25:4–16. [Google Scholar]
  • 7.Abrahams S, Fie SM, Patricios J, Posthumus M, September AV. Risk factors for sports concussion: an evidence-based systematic review. Br J Sports Med. 2014;48:91–97. doi: 10.1136/bjsports-2013-092734. [DOI] [PubMed] [Google Scholar]
  • 8.Asplund CA, McKeag DB, Olsen CH. Sport-related concussion: factors associated with prolonged return to play. Clin J Sport Med. 2004;14:339–343. doi: 10.1097/00042752-200411000-00003. [DOI] [PubMed] [Google Scholar]
  • 9.Chrisman SP, Rivara FP, Schiff MA, Zhou C, Comstock RD. Risk factors for concussive symptoms 1 week or longer in high school athletes. Brain Inj. 2013;27:1–9. doi: 10.3109/02699052.2012.722251. [DOI] [PubMed] [Google Scholar]
  • 10.Collins MW, Iverson GL, Lovell MR, McKeag DB, Norwig J, Maroon J. On-field predictors of neuropsychological and symptom deficit following sports-related concussion. Clin J Sport Med. 2003;13:222–229. doi: 10.1097/00042752-200307000-00005. [DOI] [PubMed] [Google Scholar]
  • 11.Kontos AP, Elbin RJ, Lau B, et al. Posttraumatic migraine as a predictor of recovery and cognitive impairment after sport-related concussion. Am J Sports Med. 2013;41:1497–1504. doi: 10.1177/0363546513488751. [DOI] [PubMed] [Google Scholar]
  • 12.Kostyun RO, Hafeez I. Protracted recovery from a concussion: a focus on gender and treatment interventions in an adolescent population. Sports Health. 2015;7:52–57. doi: 10.1177/1941738114555075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Schneider KJ, Iverson GL, Emery CA, McCrory P, Herring SA, Meeuwisse WH. The effects of rest and treatment following sport-related concussion: a systematic review of the literature. Br J Sports Med. 2013;47:304–307. doi: 10.1136/bjsports-2013-092190. [DOI] [PubMed] [Google Scholar]
  • 14.Buckley TA, Munkasy BA, Clouse BP. Acute Cognitive and Physical Rest May Not Improve Concussion Recovery Time. J Head Trauma Rehabil. 2016;31(4):233–241. doi: 10.1097/HTR.0000000000000165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Moser RS, Schatz P, Glenn M, Kollias KE, Iverson GL. Examining prescribed rest as treatment for adolescents who are slow to recover from concussion. Brain Inj. 2015;29:58–63. doi: 10.3109/02699052.2014.964771. [DOI] [PubMed] [Google Scholar]
  • 16.Broglio SP, Collins MW, Williams RM, Mucha A, Kontos AP. Current and emerging rehabilitation for concussion: a review of the evidence. Clin Sports Med. 2015;34:213–231. doi: 10.1016/j.csm.2014.12.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport, Zurich, November 2012. J Athl Train. 2013;48:554–575. doi: 10.4085/1062-6050-48.4.05. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Poll Harris. How knowledgeable are Americans about concussions? Assessing and recalibrating the public’s knowledge. 2015 http://rethinkconcussions.com/wp-content/uploads/2015/09/harris-poll-report.pdf.
  • 19.Smith A, Stuart M, Greenwald R, et al. Proceedings from the Ice Hockey Summit on concussion: a call to action. Clin Neuropsychol. 2011;25:689–701. doi: 10.1080/13854046.2011.586561. [DOI] [PubMed] [Google Scholar]
  • 20.Broglio SP, Cantu RC, Gioia GA, et al. National Athletic Trainers’ Association position statement: management of sport concussion. J Athl Train. 2014;49:245–265. doi: 10.4085/1062-6050-49.1.07. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Giza CC, Kutcher JS, Ashwal S, et al. Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology. 2013;80:2250–2257. doi: 10.1212/WNL.0b013e31828d57dd. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Halstead ME, Walter KD Council on Sports M, Fitness. American Academy of Pediatrics. Clinical report--sport-related concussion in children and adolescents. Pediatrics. 2010;126:597–615. doi: 10.1542/peds.2010-2005. [DOI] [PubMed] [Google Scholar]
  • 23.Harmon KG, Drezner JA, Gammons M, et al. American Medical Society for Sports Medicine position statement: concussion in sport. Br J Sports Med. 2013;47:15–26. doi: 10.1136/bjsports-2012-091941. [DOI] [PubMed] [Google Scholar]
  • 24.National Collegiate Athletic Association. Concussion guidelines. NCAA; 2013. http://www.ncaa.org/sport-science-institute/concussion-guidelines. [Google Scholar]
  • 25.Herring SA, Cantu RC, Guskiewicz KM, Putukian M, Kibler BW. Concussion and the team physician: A consensus statement-2011 update. Medicine & Science in Sports & Exercise. 2011;43:2412–2422. doi: 10.1249/MSS.0b013e3182342e64. [DOI] [PubMed] [Google Scholar]
  • 26.Halstead ME, McAvoy K, Devore CD, et al. Returning to learning following a concussion. Pediatrics. 2013;132:948–957. doi: 10.1542/peds.2013-2867. [DOI] [PubMed] [Google Scholar]
  • 27.Lynall RC, Laudner KG, Mihalik JP, Stanek JM. Concussion-assessment and -management techniques used by athletic trainers. J Athl Train. 2013;48:844–850. doi: 10.4085/1062-6050-48.6.04. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Covassin T, Elbin RJ, 3rd, Stiller-Ostrowski JL, Kontos AP. Immediate post-concussion assessment and cognitive testing (ImPACT) practices of sports medicine professionals. J Athl Train. 2009;44:639–644. doi: 10.4085/1062-6050-44.6.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Upchurch C, Morgan CD, Umfress A, Yang G, Riederer MF. Discharge instructions for youth sports-related concussions in the emergency department, 2004 to 2012. Clin J Sport Med. 2015;25:297–299. doi: 10.1097/JSM.0000000000000123. [DOI] [PubMed] [Google Scholar]
  • 30.Arbogast KB, McGinley AD, Master CL, Grady MF, Robinson RL, Zonfrillo MR. Cognitive rest and school-based recommendations following pediatric concussion: the need for primary care support tools. Clin Pediatr (Phila) 2013;52:397–402. doi: 10.1177/0009922813478160. [DOI] [PubMed] [Google Scholar]
  • 31.Majerske CW, Mihalik JP, Ren D, et al. Concussion in sports: postconcussive activity levels, symptoms, and neurocognitive performance. J Athl Train. 2008;43:265–274. doi: 10.4085/1062-6050-43.3.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Brown NJ, Mannix RC, O’Brien MJ, Gostine D, Collins MW, Meehan WP., 3rd Effect of cognitive activity level on duration of post-concussion symptoms. Pediatrics. 2014;133:e299–304. doi: 10.1542/peds.2013-2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Moser RS, Glatts C, Schatz P. Efficacy of immediate and delayed cognitive and physical rest for treatment of sports-related concussion. J Pediatr. 2012;161:922–926. doi: 10.1016/j.jpeds.2012.04.012. [DOI] [PubMed] [Google Scholar]
  • 34.Gibson S, Nigrovic LE, O’Brien M, Meehan WP., 3rd The effect of recommending cognitive rest on recovery from sport-related concussion. Brain Inj. 2013;27:839–842. doi: 10.3109/02699052.2013.775494. [DOI] [PubMed] [Google Scholar]
  • 35.Thomas DG, Apps JN, Hoffmann RG, McCrea M, Hammeke T. Benefits of strict rest after acute concussion: a randomized controlled trial. Pediatrics. 2015;135:213–223. doi: 10.1542/peds.2014-0966. [DOI] [PubMed] [Google Scholar]
  • 36.Schnadower D, Vazquez H, Lee J, Dayan P, Roskind CG. Controversies in the evaluation and management of minor blunt head trauma in children. Curr Opin Pediatr. 2007;19:258–264. doi: 10.1097/MOP.0b013e3281084e85. [DOI] [PubMed] [Google Scholar]
  • 37.Giza CC, Griesbach GS, Hovda DA. Experience-dependent behavioral plasticity is disturbed following traumatic injury to the immature brain. Behav Brain Res. 2005;157:11–22. doi: 10.1016/j.bbr.2004.06.003. [DOI] [PubMed] [Google Scholar]
  • 38.Griesbach GS, Hovda DA, Molteni R, Wu A, Gomez-Pinilla F. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience. 2004;125:129–139. doi: 10.1016/j.neuroscience.2004.01.030. [DOI] [PubMed] [Google Scholar]
  • 39.Leddy J, Hinds A, Sirica D, Willer B. The Role of Controlled Exercise in Concussion Management. PM R. 2016;8:S91–S100. doi: 10.1016/j.pmrj.2015.10.017. [DOI] [PubMed] [Google Scholar]
  • 40.Malmivaara A, Hakkinen U, Aro T, et al. The treatment of acute low back pain--bed rest, exercises, or ordinary activity? N Engl J Med. 1995;332:351–355. doi: 10.1056/NEJM199502093320602. [DOI] [PubMed] [Google Scholar]
  • 41.Deyo RA, Diehl AK, Rosenthal M. How many days of bed rest for acute low back pain? A randomized clinical trial. N Engl J Med. 1986;315:1064–1070. doi: 10.1056/NEJM198610233151705. [DOI] [PubMed] [Google Scholar]
  • 42.Relander M, Troupp H, Af Bjorkesten G. Controlled trial of treatment for cerebral concussion. Br Med J. 1972;4:777–779. doi: 10.1136/bmj.4.5843.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.de Kruijk JR, Leffers P, Meerhoff S, Rutten J, Twijnstra A. Effectiveness of bed rest after mild traumatic brain injury: a randomised trial of no versus six days of bed rest. Journal of neurology, neurosurgery, and psychiatry. 2002;73:167–172. doi: 10.1136/jnnp.73.2.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Griesbach GS, Hovda DA, Molteni R, Gomez-Pinilla F. Alterations in BDNF and synapsin I within the occipital cortex and hippocampus after mild traumatic brain injury in the developing rat: reflections of injury-induced neuroplasticity. Journal of neurotrauma. 2002;19:803–814. doi: 10.1089/08977150260190401. [DOI] [PubMed] [Google Scholar]
  • 45.Kline AE, Wagner AK, Westergom BP, et al. Acute treatment with the 5-HT 1A receptor agonist 8-OH-DPAT and chronic environmental enrichment confer neurobehavioral benefit after experimental brain trauma. Behavioural brain research. 2007;177:186–194. doi: 10.1016/j.bbr.2006.11.036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Cacioppo JT, Hawkley LC, Norman GJ, Berntson GG. Social isolation. Ann N Y Acad Sci. 2011;1231:17–22. doi: 10.1111/j.1749-6632.2011.06028.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Colloca L, Finniss D. Nocebo effects, patient-clinician communication, and therapeutic outcomes. Jama. 2012;307:567–568. doi: 10.1001/jama.2012.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Ponsford JL, Ziino C, Parcell DL, et al. Fatigue and sleep disturbance following traumatic brain injury--their nature, causes, and potential treatments. J Head Trauma Rehabil. 2012;27:224–233. doi: 10.1097/HTR.0b013e31824ee1a8. [DOI] [PubMed] [Google Scholar]
  • 49.Lee MA, Fine B. Adolescent concussions. Connecticut medicine. 2010;74:149–156. [PubMed] [Google Scholar]
  • 50.Karlin AM. Concussion in the pediatric and adolescent population: “different population, different concerns”. PM R. 2011;3:S369–379. doi: 10.1016/j.pmrj.2011.07.015. [DOI] [PubMed] [Google Scholar]
  • 51.DiFazio M, Silverberg ND, Kirkwood MW, Bernier R, Iverson GL. Prolonged Activity Restriction After Concussion: Are We Worsening Outcomes? Clin Pediatr (Phila) 2015 doi: 10.1177/0009922815589914. [DOI] [PubMed] [Google Scholar]
  • 52.Cantu RC, Guskiewicz K, Register-Mihalik JK. A retrospective clinical analysis of moderate to severe athletic concussions. PM R. 2010;2:1088–1093. doi: 10.1016/j.pmrj.2010.07.483. [DOI] [PubMed] [Google Scholar]
  • 53.Covassin T, Elbin RJ, 3rd, Larson E, Kontos AP. Sex and age differences in depression and baseline sport-related concussion neurocognitive performance and symptoms. Clin J Sport Med. 2012;22:98–104. doi: 10.1097/JSM.0b013e31823403d2. [DOI] [PubMed] [Google Scholar]
  • 54.Field M, Collins MW, Lovell MR, Maroon J. Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J Pediatr. 2003;142:546–553. doi: 10.1067/mpd.2003.190. [DOI] [PubMed] [Google Scholar]
  • 55.Kostyun RO, Milewski MD, Hafeez I. Sleep disturbance and neurocognitive function during the recovery from a sport-related concussion in adolescents. Am J Sports Med. 2015;43:633–640. doi: 10.1177/0363546514560727. [DOI] [PubMed] [Google Scholar]
  • 56.Covassin T, Swanik CB, Sachs ML. Sex Differences and the Incidence of Concussions Among Collegiate Athletes. Journal of athletic training. 2003;38:238–244. [PMC free article] [PubMed] [Google Scholar]
  • 57.Eisenberg MA, Andrea J, Meehan W, Mannix R. Time interval between concussions and symptom duration. Pediatrics. 2013;132:8–17. doi: 10.1542/peds.2013-0432. [DOI] [PubMed] [Google Scholar]
  • 58.Guskiewicz KM, McCrea M, Marshall SW, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. Jama. 2003;290:2549–2555. doi: 10.1001/jama.290.19.2549. [DOI] [PubMed] [Google Scholar]
  • 59.Meehan WP, 3rd, Zhang J, Mannix R, Whalen MJ. Increasing recovery time between injuries improves cognitive outcome after repetitive mild concussive brain injuries in mice. Neurosurgery. 2012;71:885–891. doi: 10.1227/NEU.0b013e318265a439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Morgan CD, Zuckerman SL, King LE, Beaird SE, Sills AK, Solomon GS. Post-concussion syndrome (PCS) in a youth population: defining the diagnostic value and cost-utility of brain imaging. Child’s Nervous System. 2015;31:2305–2309. doi: 10.1007/s00381-015-2916-y. [DOI] [PubMed] [Google Scholar]
  • 61.Iverson GL, Brooks BL, Collins MW, Lovell MR. Tracking neuropsychological recovery following concussion in sport. Brain Inj. 2006;20:245–252. doi: 10.1080/02699050500487910. [DOI] [PubMed] [Google Scholar]
  • 62.Lovell MR, Collins MW, Iverson GL, et al. Recovery from mild concussion in high school athletes. J Neurosurg. 2003;98:296–301. doi: 10.3171/jns.2003.98.2.0296. [DOI] [PubMed] [Google Scholar]
  • 63.McClincy MP, Lovell MR, Pardini J, Collins MW, Spore MK. Recovery from sports concussion in high school and collegiate athletes. Brain Inj. 2006;20:33–39. doi: 10.1080/02699050500309817. [DOI] [PubMed] [Google Scholar]
  • 64.McCrea M, Barr WB, Guskiewicz K, et al. Standard regression-based methods for measuring recovery after sport-related concussion. J Int Neuropsychol Soc. 2005;11:58–69. doi: 10.1017/S1355617705050083. [DOI] [PubMed] [Google Scholar]
  • 65.McCrea M, Guskiewicz KM, Marshall SW, et al. Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. Jama. 2003;290:2556–2563. doi: 10.1001/jama.290.19.2556. [DOI] [PubMed] [Google Scholar]
  • 66.Henry LC, Elbin RJ, Collins MW, Marchetti G, Kontos AP. Examining Recovery Trajectories After Sport-Related Concussion With a Multimodal Clinical Assessment Approach. Neurosurgery. 2015 doi: 10.1227/NEU.0000000000001041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.Pellman EJ, Lovell MR, Viano DC, Casson IR. Concussion in professional football: recovery of NFL and high school athletes assessed by computerized neuropsychological testing--Part 12. Neurosurgery. 2006;58:263–274. doi: 10.1227/01.NEU.0000200272.56192.62. discussion 263–274. [DOI] [PubMed] [Google Scholar]
  • 68.Broglio SP, Puetz TW. The effect of sport concussion on neurocognitive function, self-report symptoms and postural control : a meta-analysis. Sports Med. 2008;38:53–67. doi: 10.2165/00007256-200838010-00005. [DOI] [PubMed] [Google Scholar]
  • 69.McCrea M, Iverson GL, Echemendia RJ, Makdissi M, Raftery M. Day of injury assessment of sport-related concussion. Br J Sports Med. 2013;47:272–284. doi: 10.1136/bjsports-2013-092145. [DOI] [PubMed] [Google Scholar]
  • 70.Prichep LS, McCrea M, Barr W, Powell M, Chabot RJ. Time course of clinical and electrophysiological recovery after sport-related concussion. J Head Trauma Rehabil. 2013;28:266–273. doi: 10.1097/HTR.0b013e318247b54e. [DOI] [PubMed] [Google Scholar]
  • 71.Quatman-Yates C, Hugentobler J, Ammon R, Mwase N, Kurowski B, Myer GD. The utility of the balance error scoring system for mild brain injury assessments in children and adolescents. Phys Sportsmed. 2014;42:32–38. doi: 10.3810/psm.2014.09.2073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Fazio VC, Lovell MR, Pardini JE, Collins MW. The relation between post concussion symptoms and neurocognitive performance in concussed athletes. NeuroRehabilitation. 2007;22:207–216. [PubMed] [Google Scholar]
  • 73.Makdissi M, Cantu RC, Johnston KM, McCrory P, Meeuwisse WH. The difficult concussion patient: what is the best approach to investigation and management of persistent (>10 days) postconcussive symptoms? Br J Sports Med. 2013;47:308–313. doi: 10.1136/bjsports-2013-092255. [DOI] [PubMed] [Google Scholar]
  • 74.Eisenberg MA, Meehan WP, 3rd, Mannix R. Duration and course of post-concussive symptoms. Pediatrics. 2014;133:999–1006. doi: 10.1542/peds.2014-0158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Lau B, Lovell MR, Collins MW, Pardini J. Neurocognitive and symptom predictors of recovery in high school athletes. Clinical Journal of Sport Medicine. 2009;19:216–221. doi: 10.1097/JSM.0b013e31819d6edb. [DOI] [PubMed] [Google Scholar]
  • 76.Lau BC, Collins MW, Lovell MR. Cutoff scores in neurocognitive testing and symptom clusters that predict protracted recovery from concussions in high school athletes. Neurosurgery. 2012;70:371–379. doi: 10.1227/NEU.0b013e31823150f0. discussion 379. [DOI] [PubMed] [Google Scholar]
  • 77.Meehan WP, 3rd, Mannix RC, Stracciolini A, Elbin RJ, Collins MW. Symptom severity predicts prolonged recovery after sport-related concussion, but age and amnesia do not. J Pediatr. 2013;163:721–725. doi: 10.1016/j.jpeds.2013.03.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Collins MW, Grindel SH, Lovell MR, et al. Relationship between concussion and neuropsychological performance in college football players. Jama. 1999;282:964–970. doi: 10.1001/jama.282.10.964. [DOI] [PubMed] [Google Scholar]
  • 79.Covassin T, Elbin RJ, Nakayama Y. Tracking neurocognitive performance following concussion in high school athletes. Phys Sportsmed. 2010;38:87–93. doi: 10.3810/psm.2010.12.1830. [DOI] [PubMed] [Google Scholar]
  • 80.Belanger HG, Vanderploeg RD. The neuropsychological impact of sports-related concussion: a meta-analysis. J Int Neuropsychol Soc. 2005;11:345–357. doi: 10.1017/s1355617705050411. [DOI] [PubMed] [Google Scholar]
  • 81.Dean PJ, Sato JR, Vieira G, McNamara A, Sterr A. Long-term structural changes after mTBI and their relation to post-concussion symptoms. Brain Inj. 2015:1–8. doi: 10.3109/02699052.2015.1035334. [DOI] [PubMed] [Google Scholar]
  • 82.Lange RT, Panenka WJ, Shewchuk JR, et al. Diffusion tensor imaging findings and postconcussion symptom reporting six weeks following mild traumatic brain injury. Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists. 2015;30:7–25. doi: 10.1093/arclin/acu060. [DOI] [PubMed] [Google Scholar]
  • 83.Zhu DC, Covassin T, Nogle S, et al. A potential biomarker in sports-related concussion: brain functional connectivity alteration of the default-mode network measured with longitudinal resting-state fMRI over thirty days. Journal of neurotrauma. 2015;32:327–341. doi: 10.1089/neu.2014.3413. [DOI] [PubMed] [Google Scholar]
  • 84.Dikmen SS, Corrigan JD, Levin HS, Machamer J, Stiers W, Weisskopf MG. Cognitive outcome following traumatic brain injury. J Head Trauma Rehabil. 2009;24:430–438. doi: 10.1097/HTR.0b013e3181c133e9. [DOI] [PubMed] [Google Scholar]
  • 85.Alsalaheen BA, Mucha A, Morris LO, et al. Vestibular rehabilitation for dizziness and balance disorders after concussion. J Neurol Phys Ther. 2010;34:87–93. doi: 10.1097/NPT.0b013e3181dde568. [DOI] [PubMed] [Google Scholar]
  • 86.Broshek DK, Kaushik T, Freeman JR, Erlanger D, Webbe F, Barth JT. Sex differences in outcome following sports-related concussion. J Neurosurg. 2005;102:856–863. doi: 10.3171/jns.2005.102.5.0856. [DOI] [PubMed] [Google Scholar]
  • 87.Covassin T, Elbin RJ, Bleecker A, Lipchik A, Kontos AP. Are there differences in neurocognitive function and symptoms between male and female soccer players after concussions? Am J Sports Med. 2013;41:2890–2895. doi: 10.1177/0363546513509962. [DOI] [PubMed] [Google Scholar]
  • 88.Frommer LJ, Gurka KK, Cross KM, Ingersoll CD, Comstock RD, Saliba SA. Sex differences in concussion symptoms of high school athletes. Journal of athletic training. 2011;46:76–84. doi: 10.4085/1062-6050-46.1.76. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.Collins MW, Lovell MR, Iverson GL, Cantu RC, Maroon JC, Field M. Cumulative effects of concussion in high school athletes. Neurosurgery. 2002;51:1175–1179. doi: 10.1097/00006123-200211000-00011. discussion 1180–1171. [DOI] [PubMed] [Google Scholar]
  • 90.Colvin AC, Mullen J, Lovell MR, West RV, Collins MW, Groh M. The role of concussion history and gender in recovery from soccer-related concussion. Am J Sports Med. 2009;37:1699–1704. doi: 10.1177/0363546509332497. [DOI] [PubMed] [Google Scholar]
  • 91.Covassin T, Stearne D, Elbin R. Concussion history and postconcussion neurocognitive performance and symptoms in collegiate athletes. Journal of athletic training. 2008;43:119–124. doi: 10.4085/1062-6050-43.2.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92.Guskiewicz KM, Marshall SW, Bailes J, et al. Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery. 2005;57:719–726. doi: 10.1093/neurosurgery/57.4.719. discussion 719–726. [DOI] [PubMed] [Google Scholar]
  • 93.Iverson GL, Gaetz M, Lovell MR, Collins MW. Cumulative effects of concussion in amateur athletes. Brain Inj. 2004;18:433–443. doi: 10.1080/02699050310001617352. [DOI] [PubMed] [Google Scholar]
  • 94.Heyer GL, Young JA, Rose SC, McNally KA, Fischer AN. Post-traumatic headaches correlate with migraine symptoms in youth with concussion. Cephalalgia. 2015 doi: 10.1177/0333102415590240. [DOI] [PubMed] [Google Scholar]
  • 95.Kontos AP, Covassin T, Elbin RJ, Parker T. Depression and neurocognitive performance after concussion among male and female high school and collegiate athletes. Arch Phys Med Rehabil. 2012;93:1751–1756. doi: 10.1016/j.apmr.2012.03.032. [DOI] [PubMed] [Google Scholar]
  • 96.Covassin T, Crutcher B, Bleecker A, Heiden EO, Dailey A, Yang J. Postinjury anxiety and social support among collegiate athletes: a comparison between orthopaedic injuries and concussions. Journal of athletic training. 2014;49:462–468. doi: 10.4085/1062-6059-49.2.03. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Nelson LD, Guskiewicz KM, Marshall SW, et al. Multiple Self-Reported Concussions Are More Prevalent in Athletes With ADHD and Learning Disability. Clin J Sport Med. 2015 doi: 10.1097/JSM.0000000000000207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98.Sufrinko A, Johnson EW, Henry LC. The Influence of Sleep Duration and Sleep-Related Symptoms on Baseline Neurocognitive Performance Among Male and Female High School Athletes. Neuropsychology. 2015 doi: 10.1037/neu0000250. [DOI] [PubMed] [Google Scholar]
  • 99.Custer A, Sufrinko AS, Elbin RJ, Covassin T, Collins MW, Kontos AP. Do athletes with high post-concussion symptoms scores at baseline experience worse outcomes following a concussion? Journal of Athletic Training. doi: 10.4085/1062-6050-51.2.12. In Press. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 100.Collins MW, Field M, Lovell MR, et al. Relationship between postconcussion headache and neuropsychological test performance in high school athletes. Am J Sports Med. 2003;31:168–173. doi: 10.1177/03635465030310020301. [DOI] [PubMed] [Google Scholar]
  • 101.Erlanger D, Kaushik T, Cantu R, et al. Symptom-based assessment of the severity of a concussion. J Neurosurg. 2003;98:477–484. doi: 10.3171/jns.2003.98.3.0477. [DOI] [PubMed] [Google Scholar]
  • 102.Lau BC, Kontos AP, Collins MW, Mucha A, Lovell MR. Which on-field signs/symptoms predict protracted recovery from sport-related concussion among high school football players? The American journal of sports medicine. 2011;39:2311–2318. doi: 10.1177/0363546511410655. [DOI] [PubMed] [Google Scholar]
  • 103.Mihalik JP, Register-Mihalik J, Kerr ZY, Marshall SW, McCrea MC, Guskiewicz KM. Recovery of posttraumatic migraine characteristics in patients after mild traumatic brain injury. Am J Sports Med. 2013;41:1490–1496. doi: 10.1177/0363546513487982. [DOI] [PubMed] [Google Scholar]
  • 104.Mihalik JP, Stump JE, Collins MW, Lovell MR, Field M, Maroon JC. Posttraumatic migraine characteristics in athletes following sports-related concussion. J Neurosurg. 2005;102:850–855. doi: 10.3171/jns.2005.102.5.0850. [DOI] [PubMed] [Google Scholar]
  • 105.Casson IR, Sethi NK, Meehan WP., 3rd Early symptom burden predicts recovery after sport-related concussion. Neurology. 2015;85:110–111. doi: 10.1212/WNL.0000000000001700. [DOI] [PubMed] [Google Scholar]
  • 106.Merritt VC, Arnett PA. Premorbid predictors of postconcussion symptoms in collegiate athletes. J Clin Exp Neuropsychol. 2014;36:1098–1111. doi: 10.1080/13803395.2014.983463. [DOI] [PubMed] [Google Scholar]
  • 107.Kontos AP, Elbin RJ, Kotwal RS, et al. The effects of combat-related mild traumatic brain injury (mTBI): Does blast mTBI history matter? J Trauma Acute Care Surg. 2015;79:S146–151. doi: 10.1097/TA.0000000000000667. [DOI] [PubMed] [Google Scholar]
  • 108.Broglio SP, Eckner JT, Kutcher JS. Field-based measures of head impacts in high school football athletes. Current opinion in pediatrics. 2012;24:702–708. doi: 10.1097/MOP.0b013e3283595616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 109.Broglio SP, Eckner JT, Martini D, Sosnoff JJ, Kutcher JS, Randolph C. Cumulative head impact burden in high school football. Journal of neurotrauma. 2011;28:2069–2078. doi: 10.1089/neu.2011.1825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 110.Broglio SP, Eckner JT, Surma T, Kutcher JS. Post-concussion cognitive declines and symptomatology are not related to concussion biomechanics in high school football players. Journal of neurotrauma. 2011;28:2061–2068. doi: 10.1089/neu.2011.1905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 111.Eckner JT, Sabin M, Kutcher JS, Broglio SP. No evidence for a cumulative impact effect on concussion injury threshold. Journal of neurotrauma. 2011;28:2079–2090. doi: 10.1089/neu.2011.1910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 112.Guskiewicz KM, Mihalik JP. Biomechanics of sport concussion: quest for the elusive injury threshold. Exerc Sport Sci Rev. 2011;39:4–11. doi: 10.1097/JES.0b013e318201f53e. [DOI] [PubMed] [Google Scholar]
  • 113.Reddy CC, Collins M, Lovell M, Kontos AP. Efficacy of amantadine treatment on symptoms and neurocognitive performance among adolescents following sports-related concussion. J Head Trauma Rehabil. 2013;28:260–265. doi: 10.1097/HTR.0b013e318257fbc6. [DOI] [PubMed] [Google Scholar]
  • 114.Collins MW, Kontos AP, Reynolds E, Murawski CD, Fu FH. A comprehensive, targeted approach to the clinical care of athletes following sport-related concussion. Knee Surg Sports Traumatol Arthrosc. 2014;22:235–246. doi: 10.1007/s00167-013-2791-6. [DOI] [PubMed] [Google Scholar]
  • 115.Ellis MJ, Leddy JJ, Willer B. Physiological, vestibulo-ocular and cervicogenic post-concussion disorders: an evidence-based classification system with directions for treatment. Brain Inj. 2015;29:238–248. doi: 10.3109/02699052.2014.965207. [DOI] [PubMed] [Google Scholar]
  • 116.Group TMoCmW. VA/DoD Clinical practice fuidline for management of concussion/mild traumatic brain injury. Department of Veterans Affairs DoD; 2009. [Google Scholar]
  • 117.Zemek R, Duval S, Dematteo C. Guidelines for mild traumatic brain injury and persistent symptoms [online] 2013 Available at: http://onf.org/documents/guidelines-for-concussion-mtbi-persistent-symptoms-second-edition.
  • 118.Zemek R, Duval S, Dematteo C. Guidelines for concussion/mTBI & persistant symptoms [online] 2011 Available at: http://onf.org/documents/guidelines-for-concussion-mtbi-persistent-symptoms.
  • 119.Zemek RDS, Dematteo C. Guidelines for Diagnosing and Managing Pediatric Concussion [online] 2014 Available at: http://www.onf.org/documents/guidelines-for-pediatric-concussion.
  • 120.Bloom J, Blount JG. Sideline evaluation of concussion [online] Available at: http://www.uptodate.com/contents/sideline-evaluation-of-concussion.
  • 121.Elbin RJ, Schatz P, Lowder HB, Kontos AP. An empirical review of treatment and rehabilitation approaches used in the acute, sub-acute, and chronic phases of recovery following sports-related concussion. Curr Treat Options Neurol. 2014;16:320. doi: 10.1007/s11940-014-0320-7. [DOI] [PubMed] [Google Scholar]
  • 122.Bleiberg J, Cernich AN, Cameron K, et al. Duration of cognitive impairment after sports concussion. Neurosurgery. 2004;54:1073–1078. doi: 10.1227/01.neu.0000118820.33396.6a. discussion 1078–1080. [DOI] [PubMed] [Google Scholar]
  • 123.Guskiewicz KM, Ross SE, Marshall SW. Postural Stability and Neuropsychological Deficits After Concussion in Collegiate Athletes. Journal of athletic training. 2001;36:263–273. [PMC free article] [PubMed] [Google Scholar]
  • 124.Iverson GL, Lovell MR, Collins MW. Interpreting change on ImPACT following sport concussion. The Clinical neuropsychologist. 2003;17:460–467. doi: 10.1076/clin.17.4.460.27934. [DOI] [PubMed] [Google Scholar]
  • 125.Moser RS, Iverson GL, Echemendia RJ, et al. Neuropsychological evaluation in the diagnosis and management of sports-related concussion. Arch Clin Neuropsychol. 2007;22:909–916. doi: 10.1016/j.acn.2007.09.004. [DOI] [PubMed] [Google Scholar]
  • 126.Van Kampen DA, Lovell MR, Pardini JE, Collins MW, Fu FH. The “value added” of neurocognitive testing after sports-related concussion. The American journal of sports medicine. 2006;34:1630–1635. doi: 10.1177/0363546506288677. [DOI] [PubMed] [Google Scholar]
  • 127.Register-Mihalik JK, Mihalik JP, Guskiewicz KM. Balance deficits after sports-related concussion in individuals reporting posttraumatic headache. Neurosurgery. 2008;63:76–80. doi: 10.1227/01.NEU.0000335073.39728.CE. discussion 80–72. [DOI] [PubMed] [Google Scholar]
  • 128.Sosnoff JJ, Broglio SP, Shin S, Ferrara MS. Previous mild traumatic brain injury and postural-control dynamics. Journal of athletic training. 2011;46:85–91. doi: 10.4085/1062-6050-46.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 129.Mucha A, Collins MW, Elbin RJ, et al. A Brief Vestibular/Ocular Motor Screening (VOMS) assessment to evaluate concussions: preliminary findings. Am J Sports Med. 2014;42:2479–2486. doi: 10.1177/0363546514543775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 130.Pearce KL, Sufrinko A, Lau BC, Henry L, Collins MW, Kontos AP. Near Point of Convergence After a Sport-Related Concussion: Measurement Reliability and Relationship to Neurocognitive Impairment and Symptoms. Am J Sports Med. 2015;43:3055–3061. doi: 10.1177/0363546515606430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 131.Poltavski DV, Biberdorf D. Screening for lifetime concussion in athletes: importance of oculomotor measures. Brain Inj. 2014;28:475–485. doi: 10.3109/02699052.2014.888771. [DOI] [PubMed] [Google Scholar]
  • 132.Schneider KJ, Meeuwisse WH, Nettel-Aguirre A, et al. Cervicovestibular rehabilitation in sport-related concussion: a randomised controlled trial. Br J Sports Med. 2014;48:1294–1298. doi: 10.1136/bjsports-2013-093267. [DOI] [PubMed] [Google Scholar]
  • 133.Difiori JP, Giza CC. New techniques in concussion imaging. Current sports medicine reports. 2010;9:35–39. doi: 10.1249/JSR.0b013e3181caba67. [DOI] [PubMed] [Google Scholar]
  • 134.Toledo E, Lebel A, Becerra L, et al. The young brain and concussion: imaging as a biomarker for diagnosis and prognosis. Neuroscience & Biobehavioral Reviews. 2012;36:1510–1531. doi: 10.1016/j.neubiorev.2012.03.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 135.Yuh EL, Cooper SR, Mukherjee P, et al. Diffusion tensor imaging for outcome prediction in mild traumatic brain injury: a TRACK-TBI study. J Neurotrauma. 2014;31:1457–1477. doi: 10.1089/neu.2013.3171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 136.Echemendia RJ, Iverson GL, McCrea M, et al. Advances in neuropsychological assessment of sport-related concussion. Br J Sports Med. 2013;47:294–298. doi: 10.1136/bjsports-2013-092186. [DOI] [PubMed] [Google Scholar]
  • 137.Kontos AP, McAllister-Deitrick J, Reynolds E. Mental health implications and consequences following sport-related concussion. British Journal of Sports Medicine. doi: 10.1136/bjsports-2015-095564. In Press. [DOI] [PubMed] [Google Scholar]
  • 138.Reynolds E, Collins MW, Mucha A, Troutman-Ensecki C. Establishing a clinical service for the management of sports-related concussions. Neurosurgery. 2014;75(Suppl 4):S71–81. doi: 10.1227/NEU.0000000000000471. [DOI] [PubMed] [Google Scholar]
  • 139.Stewart GW, McQueen-Borden E, Bell RA, Barr T, Juengling J. Comprehensive assessment and management of athletes with sport concussion. International journal of sports physical therapy. 2012;7:433–447. [PMC free article] [PubMed] [Google Scholar]
  • 140.Wilkins SA, Shannon CN, Brown ST, et al. Establishment of a multidisciplinary concussion program: impact of standardization on patient care and resource utilization. J Neurosurg Pediatr. 2014;13:82–89. doi: 10.3171/2013.10.PEDS13241. [DOI] [PubMed] [Google Scholar]
  • 141.Leddy JJ, Baker JG, Willer B. Active Rehabilitation of Concussion and Post-concussion Syndrome. Phys Med Rehabil Clin N Am. 2016;27:437–454. doi: 10.1016/j.pmr.2015.12.003. [DOI] [PubMed] [Google Scholar]
  • 142.Kurowski BG, Hugentobler J, Quatman-Yates C, et al. Aerobic Exercise for Adolescents With Prolonged Symptoms After Mild Traumatic Brain Injury: An Exploratory Randomized Clinical Trial. J Head Trauma Rehabil. 2016 doi: 10.1097/HTR.0000000000000238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 143.Thiagarajan P, Ciuffreda KJ. Versional eye tracking in mild traumatic brain injury (mTBI): effects of oculomotor training (OMT) Brain Inj. 2014;28:930–943. doi: 10.3109/02699052.2014.888761. [DOI] [PubMed] [Google Scholar]
  • 144.Alsalaheen BA, Whitney SL, Mucha A, Morris LO, Furman JM, Sparto PJ. Exercise prescription patterns in patients treated with vestibular rehabilitation after concussion. Physiotherapy research international : the journal for researchers and clinicians in physical therapy. 2013;18:100–108. doi: 10.1002/pri.1532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 145.Ciuffreda KJ, Rutner D, Kapoor N, Suchoff IB, Craig S, Han ME. Vision therapy for oculomotor dysfunctions in acquired brain injury: a retrospective analysis. Optometry (St Louis, Mo) 2008;79:18–22. doi: 10.1016/j.optm.2007.10.004. [DOI] [PubMed] [Google Scholar]
  • 146.Glang AE, Koester MC, Chesnutt JC, et al. The effectiveness of a web-based resource in improving postconcussion management in high schools. J Adolesc Health. 2015;56:91–97. doi: 10.1016/j.jadohealth.2014.08.011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 147.Ponsford J, Willmott C, Rothwell A, et al. Impact of early intervention on outcome following mild head injury in adults. Journal of neurology, neurosurgery, and psychiatry. 2002;73:330–332. doi: 10.1136/jnnp.73.3.330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 148.Ponsford J, Willmott C, Rothwell A, et al. Impact of early intervention on outcome after mild traumatic brain injury in children. Pediatrics. 2001;108:1297–1303. doi: 10.1542/peds.108.6.1297. [DOI] [PubMed] [Google Scholar]
  • 149.Zuckerbraun NS, Atabaki S, Collins MW, Thomas D, Gioia GA. Use of modified acute concussion evaluation tools in the emergency department. Pediatrics. 2014;133:635–642. doi: 10.1542/peds.2013-2600. [DOI] [PubMed] [Google Scholar]
  • 150.Frasca D, Tomaszczyk J, McFadyen BJ, Green RE. Traumatic brain injury and post-acute decline: what role does environmental enrichment play? A scoping review Frontiers in human neuroscience. 2013;7:31. doi: 10.3389/fnhum.2013.00031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 151.Kovesdi E, Gyorgy AB, Kwon SK, et al. The effect of enriched environment on the outcome of traumatic brain injury; a behavioral, proteomics, and histological study. Front Neurosci. 2011;5:42. doi: 10.3389/fnins.2011.00042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 152.Nithianantharajah J, Hannan AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nature reviews Neuroscience. 2006;7:697–709. doi: 10.1038/nrn1970. [DOI] [PubMed] [Google Scholar]
  • 153.Diamond MC, Ingham CA, Johnson RE, Bennett EL, Rosenzweig MR. Effects of environment on morphology of rat cerebral cortex and hippocampus. Journal of neurobiology. 1976;7:75–85. doi: 10.1002/neu.480070108. [DOI] [PubMed] [Google Scholar]
  • 154.Murtha S, Pappas BA, Raman S. Neonatal and adult forebrain norepinephrine depletion and the behavioral and cortical thickening effects of enriched/impoverished environment. Behav Brain Res. 1990;39:249–261. doi: 10.1016/0166-4328(90)90031-9. [DOI] [PubMed] [Google Scholar]
  • 155.Leddy JJ, Kozlowski K, Donnelly JP, Pendergast DR, Epstein LH, Willer B. A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clin J Sport Med. 2010;20:21–27. doi: 10.1097/JSM.0b013e3181c6c22c. [DOI] [PubMed] [Google Scholar]
  • 156.Gagnon I, Grilli L, Friedman D, Iverson G. A pilot study of active rehabilitation for adolescents who are slow to recover from sport-related concussion. Scandinavian journal of medicine & science in sports. 2015 doi: 10.1111/sms.12441. [DOI] [PubMed] [Google Scholar]
  • 157.Leddy JJ, Sandhu H, Sodhi V, Baker JG, Willer B. Rehabilitation of Concussion and Post-concussion Syndrome. Sports Health. 2012;4:147–154. doi: 10.1177/1941738111433673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 158.Silverberg ND, Iverson 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;28:250–259. doi: 10.1097/HTR.0b013e31825ad658. [DOI] [PubMed] [Google Scholar]
  • 159.Zafonte R. Diagnosis and management of sports-related concussion: a 15-year-old athlete with a concussion. Jama. 2011;306:79–86. doi: 10.1001/jama.2011.819. [DOI] [PubMed] [Google Scholar]
  • 160.Graham R, Rivara FP, Ford MA, Spicer CM. Sports-Related Concussions in Youth:: Improving the Science, Changing the Culture. National Academies Press; 2014. [PubMed] [Google Scholar]
  • 161.Bandelow B, Lichte T, Rudolf S, Wiltink J, Beutel ME. The diagnosis of and treatment recommendations for anxiety disorders. Dtsch Arztebl Int. 2014;111:473–480. doi: 10.3238/arztebl.2014.0473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 162.Brown HE, Pearson N, Braithwaite RE, Brown WJ, Biddle SJ. Physical activity interventions and depression in children and adolescents : a systematic review and meta-analysis. Sports Med. 2013;43:195–206. doi: 10.1007/s40279-012-0015-8. [DOI] [PubMed] [Google Scholar]
  • 163.Andersen LL, Mortensen OS, Zebis MK, Jensen RH, Poulsen OM. Effect of brief daily exercise on headache among adults--secondary analysis of a randomized controlled trial. Scand J Work Environ Health. 2011;37:547–550. doi: 10.5271/sjweh.3170. [DOI] [PubMed] [Google Scholar]
  • 164.Santiago MD, de Carvalho DS, Gabbai AA, Pinto MM, Moutran AR, Villa TR. Amitriptyline and aerobic exercise or amitriptyline alone in the treatment of chronic migraine: a randomized comparative study. Arq Neuropsiquiatr. 2014;72:851–855. doi: 10.1590/0004-282x20140148. [DOI] [PubMed] [Google Scholar]
  • 165.Varkey E, Cider A, Carlsson J, Linde M. Exercise as migraine prophylaxis: a randomized study using relaxation and topiramate as controls. Cephalalgia. 2011;31:1428–1438. doi: 10.1177/0333102411419681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 166.Baker JG, Freitas MS, Leddy JJ, Kozlowski KF, Willer BS. Return to full functioning after graded exercise assessment and progressive exercise treatment of postconcussion syndrome. Rehabil Res Pract. 2012;2012:705309. doi: 10.1155/2012/705309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 167.Yang J, Peek-Asa C, Covassin T, Torner JC. Post-concussion symptoms of depression and anxiety in division I collegiate athletes. Dev Neuropsychol. 2015;40:18–23. doi: 10.1080/87565641.2014.973499. [DOI] [PubMed] [Google Scholar]
  • 168.Covassin T, Moran R, Wilhelm K. Concussion symptoms and neurocognitive performance of high school and college athletes who incur multiple concussions. Am J Sports Med. 2013;41:2885–2889. doi: 10.1177/0363546513499230. [DOI] [PubMed] [Google Scholar]
  • 169.Mainwaring LM, Hutchison M, Bisschop SM, Comper P, Richards DW. Emotional response to sport concussion compared to ACL injury. Brain Inj. 2010;24:589–597. doi: 10.3109/02699051003610508. [DOI] [PubMed] [Google Scholar]
  • 170.Gioia GA, Glang AE, Hooper SR, Eagan Brown B. Building statewide infrastructure for the academic support of students with mild traumatic brain injury. Journal of Head Trauma Rehabilitation. doi: 10.1097/HTR.0000000000000205. In Press. [DOI] [PubMed] [Google Scholar]
  • 171.Ransom DM, Vaughan CG, Pratson L, Sady MD, McGill CA, Gioia GA. Academic effects of concussion in children and adolescents. Pediatrics. 2015;135:1043–1050. doi: 10.1542/peds.2014-3434. [DOI] [PubMed] [Google Scholar]
  • 172.Center for Disease Control. HEADS UP to School Sports. 2015 http://www.cdc.gov/headsup/highschoolsports/index.html.
  • 173.McAvoy K. Concussion RMSMICf, editor. REAP the benefits of good concussion management. http://wwwconcussiontreatmentcom/images/REAP_Programpdf. Centennial, CO2009.
  • 174.Brown BE, Vaccaro M. Brain Injury. Informa Healthcare; Telephone House, 69–77 Paul Street, London Ec2a 4lq, England: 2014. Pennsylvania’s BrainSTEPS Program: The Return to School & Academics Statewide Concussion Management Team (CMT) Project; pp. 838–839. [Google Scholar]
  • 175.Center for Disease Control. HEADS UP to Providers. 2015 http://www.cdc.gov/headsup/providers/index.html.

RESOURCES