You are here

Article Text

Article menu
Review
Day of injury assessment of sport-related concussion
  1. Michael McCrea1,
  2. Grant L Iverson2,
  3. Ruben J Echemendia3,
  4. Michael Makdissi4,
  5. Martin Raftery5
  1. 1Departments of Neurosurgery and Neurology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA
  2. 2Department of Psychiatry, University of British Columbia, Vancouver, British Columbia, Canada
  3. 3University of Missouri-Kansas City, Psychological and Neurobehavioral Associates, Inc., State College, Pennsylvania, USA
  4. 4The Florey Institute of Neuroscience and Mental Health, Melbourne Brain Centre, Melbourne, Australia
  5. 5International Rugby Board, New South Wales, Australia
  1. Correspondence to Dr Michael McCrea, Departments of Neurosurgery and Neurology, Medical College of Wisconsin, Milwaukee, WI 53226, USA; mmccrea{at}mcw.edu

Abstract

Objective To conduct a critical review of the literature on instruments currently used in the assessment of sport-related concussion on the day of injury.

Data sources Computerised searches of the literature posted to MEDLINE, PubMed, CINAHL, PsychInfo and Cochrane Library from 1 January 1982 through 21 August 2012. Key words and medical embedded subheadings (MeSH) terms relevant to sport-related concussion were applied, which identified 577 articles.

Study selection In addition to MeSH term and key word criteria, a study was included in the analysis if the article: (1) was published in English, (2) represented original research, (3) pertained to sport-related concussion (ie, not non-sports traumatic brain injury), (4) included assessment or diagnostic data collected within 24 h of the injury event and (5) involved human research. A total of 41 studies qualified for review.

Data extraction All articles were examined to determine if the study met the additional requirements for inclusion. A standardised method was used to document critical elements of the study design, population, tests employed and key findings.

Data synthesis A large number of studies were analysed that reported data from testing conducted within 24 h of injury. These studies collectively demonstrated that a number of instruments are capable of measuring the acute effects of concussion across several domains, such as symptoms, cognition and balance.

Results Relating to specific assessment domains are compiled in separate tables and an interpretive summary of the findings is provided.

Conclusions Several well-validated tests are appropriate for use in the assessment of acute concussion in the competitive sporting environment. These tests provide important data on the symptoms and functional impairments that clinicians can incorporate into their diagnostic formulation, but they should not solely be used to diagnose concussion.

  • Concussion
  • Contact sports
  • Head injuries

https://doi.org/10.1136/bjsports-2013-092145

Statistics from Altmetric.com

    Request Permissions

    If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

    Introduction

    Concussion is often considered by clinicians to be among the most complex injuries in sports medicine to diagnose, assess and manage. There is no perfect diagnostic test or marker for an immediate diagnosis of concussion in the sporting environment. Rather, it is a clinical diagnosis based largely on the observed injury mechanism, signs and symptoms. A vast majority of sport-related concussions (hereafter referred to as concussion) occur without loss of consciousness or frank neurological signs.1–4 In milder forms of concussion, the athlete might be slightly confused, without clearly identifiable retrograde or post-traumatic amnesia. In addition, most concussions cannot be identified or diagnosed by neuroimaging techniques (eg, CT orMRI).

    Over the past two decades, there has been a concentrated, international effort towards improved methods for diagnosing concussion. Subject matter experts have attempted to build consensus on the key signs and symptoms critical to the diagnosis, particularly during the acute postinjury period.5 ,6 Sport governing bodies have sponsored global educational campaigns to make athletes, parents, clinicians and other key stakeholders better able to recognise the signs and symptoms that indicate possible concussion.

    At the same time, a ‘standardisation movement’ has facilitated the development of several tests designed to aid in concussion assessment and diagnosis. A basic premise of this movement has been that performance-based assessment measures may be superior to an athlete's reporting of symptoms, which might be unreliable due to the athlete's tendency to under-report or fail to recognise their symptoms. Standardised tests are intended to provide a more objective, performance-based method of measuring postinjury recovery and determining an athlete's fitness to return to play. In most cases, these tests assess single domains of concussion effects (eg, postconcussion symptoms, neurocognitive functioning and postural stability). The recently developed Sports Concussion Assessment Tool—Second Edition (SCAT2)7 involves an integrated, multimodal assessment model. In addition to brief screening tests, there has been a proliferation in recent years of computerised neurocognitive tests proposed for concussion assessment.

    Standardised tests and measures can be used on the day of injury to assess the acute effects of injury. The purpose of this article is to describe the methods and results of a critical review intended to specifically address whether the existing tests and measures currently in use are sensitive and reliable enough on the day of injury to assist clinicians in accurately evaluating sport-related concussion.

    Methods

    Literature search

    We conducted a systematic survey of the published literature in several computerised databases, including: MEDLINE, PubMed, CINAHL, PsychInfo and Cochrane Library. Based on the focus of this critical review, we limited our search to the published literature over a 30-year period from 1 January 1982 through 21 August 2012. We used a combination of the following key words and medical embedded subheadings (MeSH) terms as parameters for our search:

    • 1. Concuss* (concussion, concussed, concussive, etc), Brain Inj* (brain injury, injuries, injured, etc), Head Inj* (head injury, injuries, injured, etc);

    • 2. Sport*, athlete*, football, soccer, ice hockey, field hockey, boxing, rugby, lacrosse, wrestling;

    • 3. Diagnos*, assess*, test*.

    Terms within each group were combined using the Boolean operator ‘OR’; then the two groups were combined using the Boolean ‘AND’ operator. Search statistics were documented with respect to the number of articles generated by the MeSH term and key word search. In addition, the reference lists of acquired articles of relevance were reviewed for other articles not found in the electronic databases.

    Study selection criteria

    In addition to meeting the MeSH term and key word search criteria, the basic requirements for a study to be included were that the article: (1) was published in English, (2) represented original research, (3) pertained to sport-related concussion (ie, not non-sports traumatic brain injury), (4) included assessment or diagnostic data collected on the day of injury (eg, within 24 h of the injury event) and (5) involved human research (no animal studies). Duplicate articles from more than one electronic database were eliminated.

    Data extraction and analysis

    Each article identified by the electronic literature search was reviewed to determine if it met the inclusion criteria described above. In some instances, this determination could be made from a review of the abstract. In other cases, it required a review of the full-text article. For the included studies, a standardised data extraction method was used to document the study design, population and assessment techniques (see Tables 1⇓⇓⇓⇓–6). For each study, the reviewer provided a summary of the key findings, statistics and a critical assessment of the evidence relevant to the day of injury assessment. We did not conduct a detailed or systematic analysis of the psychometric properties of the instruments included in this review.

    View this table:
    Table 1

    Studies using symptom checklists on the day of injury

    Results

    In total, the electronic literature database search identified 577 articles. After applying additional requirements and eliminating duplicate articles, a total of 44 qualified for further review. A majority of articles were rejected because data were not collected within 24 h of the injury. Several studies included assessments across multiple domains (eg, symptoms, cognition and balance) and were included in those individual domains accordingly. Tables 1⇓⇓⇓⇓–6 below provide a summary of key findings from studies in each assessment domain.

    Symptom rating scales

    Several studies have documented symptoms of concussion immediately following, or over the first 24 h after, injury. These studies usually use a symptom rating scale completed by the athlete. The most commonly and consistently reported acute symptoms, across studies, are headaches, dizziness and some form of mental status disturbance, such as mental clouding, confusion or a slowing down of feelings.8–14 Other commonly reported acute symptoms include visual problems, fatigue and nausea.8 ,11 ,13 ,14 Some observable signs of concussion include a dazed facial expression and unsteady gait.13

    Data from 18 studies that reported results from symptom rating scales in the first 24 h following injury were extracted and included in table 1. The time interval following injury varied considerably, from minutes to the following day. Research groups used many variations of concussion rating scales, which varied considerably in the number of symptoms being assessed.

    The Post-Concussion Scale15–17 has evolved over the years, and slightly different versions have been used in published studies.18–24 The internal consistency of the scale ranges from 0.88 to 0.94 in high school and college students, and from 0.92 to 0.93 in concussed athletes.25 Normative data for the scale are available for 1391 young men and 355 young women in high school or university.25

    SCAT2 is an outcome measure that includes symptom ratings, balance testing and cognitive screening.7 Two scores are derived from the SCAT2 symptom scale: total number of symptoms and symptom severity score. The symptom severity score is intuitive in that it is the sum of the Likert ratings for the entire scale. This score, however, is not included in the SCAT2 total score. The total number of symptoms score is included in the SCAT2 total score. This score is reverse scored in that the total number of symptoms endorsed as mild or greater are subtracted from 22 (thus, if a person endorses 8 symptoms, his score would be 14). A number of concerns have been expressed about the design and scoring of SCAT2, and recommendations have been offered for improving it for clinical use.26 Normative reference values are available for high school students. Data are not available on large samples of concussed athletes.

    The Concussion Symptom Inventory (CSI27) is a 12-item scale that was developed using samples of more than 16 000 uninjured athletes and more than 600 concussed athletes. It can be derived from the Post-Concussion Scale and SCAT2. A comparison of the three concussion rating scales is provided in table 2.

    View this table:
    Table 2

    Comparing three concussion symptom rating scales

    One of the most salient findings from this review is that these rating scales are sensitive to the acute effects of concussion in high school, university and professional athletes. Acutely concussed athletes, on average, obtain high scores on symptom rating scales, which is consistent with a meta-analytic review of the literature. Broglio and Puetz28 extracted data from 14 studies involving 1796 injured athletes. Across the 14 studies, the mean overall effect size an average of 1.2 days after injury was large (ie, –3.31). In 10 studies that included both symptom ratings and cognitive assessment (N=913 injured athletes), the average effect sizes for symptom ratings (–1.21) and cognition (–0.95) were more similar. Symptom checklist scores and the corresponding sensitivity of the scales typically diminish with the passage of time due to natural recovery.

    Neurocognitive tests

    A total of 31 studies using cognitive testing on the day of injury qualified for review (see table 3). Data were available from several competitive levels across a broad array of sports. Most of these studies used brief cognitive screening tests intended for rapid assessment in the sporting environment (eg, sideline and rink side). Fewer studies utilised conventional (‘paper and pencil’) neuropsychological testing within 24 h of injury, and 11 studies involved the use of computerised neuropsychological testing. The most widely studied instrument has been the Standardised Assessment of Concussion (SAC; 12 studies). ANAM (n=5), CogSport/Axon (n=3) and ImPACT (3 studies) were the most commonly studied computerised tests.

    View this table:
    Table 3

    Studies using cognitive tests on the day of injury

    The array of studies reviewed illustrates the ability to measure or quantify the nature and magnitude of cognitive impairment within the first 24 h of concussion. These studies document that neuropsychological tests can detect changes across multiple domains of cognitive functioning that are susceptible to the acute effects of concussion, such as cognitive processing speed, working memory, attention and concentration, new learning and memory and executive functioning. Measures of orientation appear less sensitive, but might be a marker of a more severe gradient of injury when impaired.

    The study by Broglio et al29 was the most extensive comparison of conventional and computerised neurocognitive testing approaches within 24 h of injury. This study revealed different levels of detecting cognitive abnormalities across ImPACT, Headminder CRI and a conventional test battery. A high percentage of symptomatic athletes exhibited a significant decline on both computerised and conventional neuropsychological testing on the day of injury. Approximately 15–30% of athletes were also impaired on testing after reporting a full symptom recovery. It should be noted, however, that 10–25% of athletes who were still symptomatic showed no significant decline on cognitive testing.

    Overall, the studies reviewed illustrated a significant decline in cognitive functioning compared with an athlete's individual preinjury baseline performance, relative to the performance of non-injured control athletes or both. This ability to detect and quantify acute cognitive impairment is evident on both brief screening measures (ie, the SAC) and conventional and computerised neuropsychological test batteries. Relatively few studies report sensitivity/specificity data on the ability of particular cognitive tests to differentiate concussed versus non-concussed athletes at the individual case level.

    Postural stability/balance tests

    Numerous studies illustrate that balance is typically affected in concussed athletes in the early postinjury period2 ,29–34 (see table 4). The majority of studies examine group data in concussed athletes compared with their own baseline and/or compared with uninjured controls.2 ,29–34 Initial studies involved the use of sophisticated computerised test platforms, which are not practical for sideline assessments. Guskiewicz and colleagues later reported that simple clinical tests (eg, Balance Error Scoring System, BESS) could also detect balance deficits following injury.34 ,35 A study by Broglio et al29 assessed the ability of balance testing to detect a significant change (defined as 1 SD below baseline) in the individual athlete following a concussion. Most, but not all, concussed athletes had significant balance deficits following injury.

    View this table:
    Table 4

    Studies using balance tests on the day of injury

    Taken together, these studies show that balance is an important component of the sideline assessment.36 ,37 Currently, SCAT2 contains a modified BESS (M-BESS) which utilises the three BESS stances on a hard surface only. Further research is required to examine the sensitivity and reliability of the M-BESS for the detection of balance deficits in concussed athletes assessed on the sidelines.

    Electrophysiological tests

    Electrophysiological measures have been used to examine athletes and non-athletes following concussion.38–40 Only recently have researchers examined the role of these measures during the acute phase of injury (see table 5). McCrea et al41 conducted a prospective non-randomised study of 28 high school and college athletes who sustained a concussion while playing football. Analyses of the qEEG data revealed significant within-group differences from baseline to the first 24 h postinjury and at 8 days postinjury. Differences between the concussed and control groups were found within the first day postinjury and at 8 days postinjury.

    View this table:
    Table 5

    Studies using electrophysiological measures on the day of injury

    Barr et al42 reported significant differences using qEEG between the injured and control groups within the first 24 h and 8 days postinjury; no differences were found between groups at 45 days. Drawing from the same cohort of athletes and using the same measures as the previous two studies, Prichep et al43 found statistically significant differences between athletes with mild and moderate concussion within 24 h, 8 days and 45 days postinjury. Sensitivity to moderate concussion was reported as 55% (95% CI 28% to 79%) and specificity was noted to be 94% (95% CI 84% to 98%) within 24 h of injury.

    Other assessment measures

    There are references in the literature and mainstream media regarding new paradigms, tests and devices in development for the intended use of assessing sport-related concussion. Only three studies in the literature included the day of injury data (see table 6). No conclusion can be drawn at this point regarding the eventual usefulness of these methods or others yet in the development pipeline.

    View this table:
    Table 6

    Studies using other assessment devices and tests on the day of injury

    Discussion

    Results from this critical review of the scientific literature inform our understanding of the acute clinical presentation of sport-related concussion and an array of tests in use for concussion assessment. Concussion clearly produces a constellation of self-reported symptoms and impairments in cognitive functioning, balance and other functional capacities during the acute phase (eg, initial 24 h). This review illustrates that clinical tests are capable of detecting and quantifying those effects on the day of injury.

    It is important to appreciate that tests do not diagnose whether a concussion has occurred. Rather, tests provide data on the physiological, cognitive, psychological and behavioral changes associated with the injury that can aid the clinician in the overall diagnostic formulation, gauging the gradient of injury severity, assessing clinical recovery and determining fitness to resume participation in sport.

    Although concerns are routinely expressed about athletes under-reporting concussion or the resulting symptoms,44 this review suggests that symptom assessment remains a critical component of concussion assessment. The studies reviewed indicate large effect sizes in self-reported symptoms on the day of injury, typically larger than the deficits seen in performance-based methods. In sum, the literature clearly supports the continued use of symptom scales in the assessment of concussed athletes, ideally in combination with other functional tests.

    This review illustrates that the effects of concussion are not confined to one domain (eg, cognitive functioning). That is, athletes, to varying degrees, experience a complex combination of symptoms and exhibit deficits across multiple domains of functioning. As a result, reliance on a single test or multiple measures in a single assessment domain will very likely be less accurate than a multimodal assessment. A multidimensional approach that integrates assessment of self-reported symptoms and other functional domains (eg, cognitive function and balance) known to be affected by concussion is recommended. The specific tests selected to form the multidimensional assessment approach not only need to be reliable and valid, but also may vary depending on the situational constraints of the sporting environment, athlete population and the experience of the assessor. SCAT2 integrates a multimodal assessment into a single outcome measure for use in the competitive sporting environment. Individual components of SCAT-2 have been the focus of recent studies, but further research is required to illustrate the reliability, sensitivity and clinical utility of the entire SCAT2.

    The evidence base on the utility of neuropsychological testing has been greatly advanced over the past two decades. Although many critical questions have been answered, further research is required to specifically address a number of important questions related to the usefulness of cognitive testing. Priorities for future study are listed below.

    • Comparing the added value of computerised versus brief cognitive screening tests on the day of injury and at subsequent assessment points.

    • Determining how the day of injury cognitive test performance might predict the course and duration of recovery (including markers indicating the risk of prolonged recovery).

    • Comparing the reliability, validity, sensitivity and specificity of baseline versus no baseline models of cognitive assessment in measuring the acute effects of concussion.

    A small number of recent studies provide preliminary data regarding the use of electrophysiological and other measures in the acute evaluation of concussion43 ,45 and suggest that physiological recovery may persist significantly beyond recovery as assessed by clinical measures (eg, symptoms, balance and cognition).41 Although these methods show promise, further research is required to support their use in the sporting environment.

    Conclusion

    Based on the complex and heterogeneous clinical presentation of concussion, a multimodal approach is recommended to maximise the sensitivity of clinical evaluation on the day of injury. This approach includes formal symptom assessment and standardised testing of cognitive ability and balance. Several tests and measures are appropriate for use in the assessment of acute concussion on the day of injury in the competitive sporting environment. These tests provide important data on the symptoms and functional impairments that clinicians can incorporate into their diagnostic formulation, but they should not solely be used to diagnose concussion. Future research should focus on the incremental value of these assessment instruments for predicting an athlete's recovery course, influencing injury management strategies and reducing risks associated with sport-related concussion.

    What are the new findings?

    • Major progress has been made towards the development and validation of standardised methods for the assessment of sport-related concussion over the past 20 years.

    • Several tests and measures are appropriate for use in the assessment of acute concussion on the day of injury in the competitive sporting environment.

    • A multimodal approach that includes formal symptom assessment and standardised testing of cognitive ability and balance is recommended to maximise the sensitivity of clinical evaluation on the day of injury.

    How might it impact on clinical practice in the near future?

    • Concussion tests provide important data on the symptoms and functional impairments that clinicians can incorporate into their diagnostic formulation, but they should not solely be used to diagnose concussion.

    • Inclusion of standardised measures will provide clinicians with a more systematic and accurate approach to concussion assessment.

    • Accurate assessment on the day of injury can drive informed clinical management and return to play decision making that improves athlete safety and outcome after sport-related concussion.

    Acknowledgments

    The authors acknowledge and appreciate the assistance of Adam Pfaller, Research Assistant in the Brain Injury Research Program at the Medical College of Wisconsin, with the literature search and data extraction for this systematic review.

    References

    1. ↵
      1. Guskiewicz KM,
      2. Weaver NL,
      3. Padua DA,
      4. et al
      . Epidemiology of concussion in collegiate and high school football players. Am J Sports Med 2000;28:643–50.
      OpenUrlAbstract/FREE Full Text
    2. ↵
      1. McCrea M,
      2. Guskiewicz KM,
      3. Marshall SW,
      4. et al
      . Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003;290:2556–63.
      OpenUrlCrossRefPubMedWeb of Science
    3. ↵
      1. Macciocchi SN,
      2. Barth JT,
      3. Alves W,
      4. et al
      . Neuropsychological functioning and recovery after mild head injury in collegiate athletes. Neurosurgery 1996;39:510–14.
      OpenUrlCrossRefPubMedWeb of Science
    4. ↵
      1. Meehan WP III.,
      2. D'hemecourt P,
      3. Comstock RD
      . High school concussions in the 2008–2009 academic year: mechanism, symptoms, and management. Am J Sports Med 2010;38:2405–9.
      OpenUrlAbstract/FREE Full Text
    5. ↵
      1. Kelly JP,
      2. Rosenberg JH
      . Diagnosis and management of concussion in sports. Neurology 1997;48:575–80.
      OpenUrlCrossRef
    6. ↵
      1. McCrory P,
      2. Johnston K,
      3. Meeuwisse W,
      4. et al
      . Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004. Br J Sports Med 2005;39:196–204.
      OpenUrlAbstract/FREE Full Text
    7. ↵
      1. McCrory P,
      2. Meeuwisse W,
      3. Johnston K,
      4. et al
      . Consensus Statement on Concussion in Sport: the 3rd International Conference on Concussion in Sport held in Zurich, November 2008. Br J Sports Med 2009;43(Suppl 1):i76–90.
      OpenUrlFREE Full Text
    8. ↵
      1. Benson BW,
      2. Meeuwisse WH,
      3. Rizos J,
      4. et al
      . A prospective study of concussions among National Hockey League players during regular season games: the NHL-NHLPA Concussion Program. CMAJ 2011;183:905–11.
      OpenUrlAbstract/FREE Full Text
    9. ↵
      1. Pellman EJ,
      2. Powell JW,
      3. Viano DC,
      4. et al
      . Concussion in professional football: epidemiological features of game injuries and review of the literature—part 3. Neurosurgery 2004;54:81–94; discussion 94–6
      OpenUrlCrossRefPubMedWeb of Science
    10. ↵
      1. Duhaime AC,
      2. Beckwith JG,
      3. Maerlender AC,
      4. et al
      . Spectrum of acute clinical characteristics of diagnosed concussions in college athletes wearing instrumented helmets. J Neurosurg 2012;117:1092–9.
      OpenUrlCrossRefPubMedWeb of Science
    11. ↵
      1. Lau BC,
      2. Kontos AP,
      3. Collins MW,
      4. et al
      . Which on-field signs/symptoms predict protracted recovery from sport-related concussion among high school football players? Am J Sports Med 2011;39:2311–18.
      OpenUrlAbstract/FREE Full Text
    12. ↵
      1. Guskiewicz KM,
      2. McCrea M,
      3. Marshall SW,
      4. et al
      . Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003;290:2549–55.
      OpenUrlCrossRefPubMedWeb of Science
    13. ↵
      1. Maddocks DL,
      2. Dicker GD,
      3. Saling MM
      . The assessment of orientation following concussion in athletes. Clin J Sport Med 1995;5:32–5.
      OpenUrlCrossRefPubMedWeb of Science
    14. ↵
      1. McCrory PR,
      2. Ariens T,
      3. Berkovic SF
      . The nature and duration of acute concussive symptoms in Australian football. Clin J Sport Med 2000;10:235–8.
      OpenUrlCrossRefPubMedWeb of Science
    15. ↵
      1. Lovell MR
      . Evaluation of the professional athlete. Paper presented at: new developments in sports-related concussion conference1996, Pittsburgh, PA.
    16. ↵
      1. Lovell MR
      . Evaluation of the professional athlete. In: Bailes JE, Lovell MR, Maroon JC, eds. Sports-related concussion. St. Louis: Quality Medical Publishing, 1999, 20014.
    17. ↵
      1. Lovell MR,
      2. Collins MW
      . Neuropsychological assessment of the college football player. J Head Trauma Rehabil 1998;13:9–26.
      OpenUrlCrossRefPubMedWeb of Science
    18. ↵
      1. Collins MW,
      2. Field M,
      3. Lovell MR,
      4. et al
      . Relationship between postconcussion headache and neuropsychological test performance in high school athletes. Am J Sports Med 2003;31:168–73.
      OpenUrlAbstract/FREE Full Text
    19. ↵
      1. Iverson GL,
      2. Gaetz M,
      3. Lovell MR,
      4. et al
      . Relation between subjective fogginess and neuropsychological testing following concussion. J Int Neuropsychol Soc 2004;10:904–6.
      OpenUrlCrossRefPubMedWeb of Science
    20. ↵
      1. Iverson GL,
      2. Gaetz M,
      3. Lovell MR,
      4. et al
      . Cumulative effects of concussion in amateur athletes. Brain Inj 2004;18:433–43.
      OpenUrlCrossRefPubMedWeb of Science
    21. ↵
      1. Lovell MR,
      2. Collins MW,
      3. Iverson GL,
      4. et al
      . Recovery from mild concussion in high school athletes. J Neurosurg 2003;98:296–301.
      OpenUrlCrossRefPubMedWeb of Science
    22. ↵
      1. Lovell MR,
      2. Collins MW,
      3. Iverson GL,
      4. et al
      . Grade 1 or “ding” concussions in high school athletes. Am J Sports Med 2004;32:47–54.
      OpenUrlAbstract/FREE Full Text
    23. ↵
      1. Lovell MR,
      2. Echemendia RJ,
      3. Burke CJ
      . Traumatic brain injury in professional hockey. In: Lovell MR, Echemendia RJ, Barth J, et al. eds. Traumatic brain injury in sports: an international neuropsychological perspective. Lisse: Swets-Zietlinger, 2004:221–31.
    24. ↵
      1. Lovell MR,
      2. Burke CJ
      . The NHL concussion program. In: Cantu R ed. Neurologic athletic head and spine injury. Philadelphia: WB Saunders, 2002:32–45.
    25. ↵
      1. Lovell MR,
      2. Iverson GL,
      3. Collins MW,
      4. et al
      . Measurement of symptoms following sports-related concussion: reliability and normative data for the post-concussion scale. Appl Neuropsychol 2006;13:166–74.
      OpenUrlCrossRefPubMed
    26. ↵
      1. Patricios J,
      2. Collins R,
      3. Branfield A,
      4. et al
      . The sports concussion note: should SCAT become SCOAT? Br J Sports Med 2012;46:198–201.
      OpenUrlAbstract/FREE Full Text
    27. ↵
      1. Randolph C,
      2. Millis S,
      3. Barr WB,
      4. et al
      . Concussion symptom inventory: an empirically derived scale for monitoring resolution of symptoms following sport-related concussion. Arch Clin Neuropsychol 2009;24:219–29.
      OpenUrlAbstract/FREE Full Text
    28. ↵
      1. Broglio SP,
      2. 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.
      OpenUrlCrossRefPubMedWeb of Science
    29. ↵
      1. Broglio SP,
      2. Macciocchi SN,
      3. Ferrara MS
      . Sensitivity of the concussion assessment battery. Neurosurgery 2007;60:1050–7; discussion 1057–8.
      OpenUrlPubMedWeb of Science
    30. ↵
      1. Guskiewicz KM
      . Postural stability assessment following concussion: one piece of the puzzle. Clin J Sport Med 2001;11:182–9.
      OpenUrlCrossRefPubMedWeb of Science
    31. ↵
      1. Peterson CL,
      2. Ferrara MS,
      3. Mrazik M,
      4. et al
      .  Evaluation of neuropsychological domain scores and postural stability following cerebral concussion in sports. Clin J Sport Med 2003;13:230–7.
      OpenUrlCrossRefPubMedWeb of Science
    32. ↵
      1. Guskiewicz KM,
      2. Perrin DH,
      3. Gansneder BM
      . Effect of mild head injury on postural stability in athletes. J Athl Train 1996;31:300–6.
      OpenUrlPubMed
    33. ↵
      1. Guskiewicz KM,
      2. Riemann BL,
      3. Perrin DH,
      4. et al
      . Alternative approaches to the assessment of mild head injury in athletes. Med Sci Sports Exerc 1997;29(7 Suppl):S213–21.
      OpenUrlPubMedWeb of Science
    34. ↵
      1. Riemann BL,
      2. Guskiewicz KM
      . Effects of mild head injury on postural stability as measured through clinical balance testing. J Athl Train 2000;35:19–25.
      OpenUrlPubMedWeb of Science
    35. ↵
      1. Guskiewicz KM,
      2. Ross SE,
      3. Marshall SW
      . Postural stability and neuropsychological deficits after concussion in collegiate athletes. J Athl Train 2001;36:263–73.
      OpenUrlPubMedWeb of Science
    36. ↵
      1. Susco TM,
      2. McLeod TC Valovich,
      3. Gansneder BM,
      4. et al
      . Balance recovers within 20 minutes after exertion as measured by the balance error scoring system. J Athl Train 2004;39:241–6.
      OpenUrlPubMedWeb of Science
    37. ↵
      1. Wilkins JC,
      2. McLeod TC Valovich,
      3. Perrin DH,
      4. et al
      . Performance on the balance error scoring system decreases after fatigue. J Athl Train 2004;39:156–61.
      OpenUrlPubMedWeb of Science
    38. ↵
      1. Slobounov S,
      2. Sebastianelli W,
      3. Hallett M
      . Residual brain dysfunction observed one year post-mild traumatic brain injury: combined EEG and balance study. Clin Neurophysiol 2012;123:1755–61.
      OpenUrlCrossRefPubMed
    39. ↵
      1. Moeller JJ,
      2. Tu B,
      3. Bazil CW
      . Quantitative and qualitative analysis of ambulatory electroencephalography during mild traumatic brain injury. Arch Neurol 2011;68:1595–8.
      OpenUrlCrossRefPubMedWeb of Science
    40. ↵
      1. Arciniegas DB
      . Clinical electrophysiologic assessments and mild traumatic brain injury: state-of-the-science and implications for clinical practice. Int J Psychophysiol 2011;82:41–52.
      OpenUrlCrossRefPubMedWeb of Science
    41. ↵
      1. McCrea M,
      2. Prichep LS,
      3. Powell MR,
      4. et al
      . Acute effects and recovery after sport-related concussion: a neurocognitive and quantitative brain electical activity study. J Head Trauma Rehabil 2010;25:283–92.
      OpenUrlCrossRefPubMedWeb of Science
    42. ↵
      1. Barr WB,
      2. Prichep LS,
      3. Chabot R,
      4. et al
      . Measuring brain electrical activity to track recovery from sport-related concussion. Brain Inj 2012;26:58–66.
      OpenUrlCrossRefPubMedWeb of Science
    43. ↵
      1. Prichep LS,
      2. McCrea M,
      3. Barr W,
      4. et al
      . Time course of clinical and electrophysiological recovery after sport-related concussion. J Head Trauma Rehabil 2012, doi:10.1097/HTR.0b013e318247b54e
    44. ↵
      1. McCrea M,
      2. Hammeke T,
      3. Olsen G,
      4. et al
      . Unreported concussion in high school football players: implications for prevention. Clin J Sport Med 2004;14:13–17.
      OpenUrlCrossRefPubMedWeb of Science
    45. ↵
      1. Barr WB,
      2. Prichep LS,
      3. Chabot R,
      4. et al
      . Measuring brain electrical activity to track recovery from sport-related concussion. Brain Inj 2012;26:58–66.
      OpenUrlCrossRefPubMedWeb of Science
      1. McCrea M,
      2. Guskiewicz K,
      3. Randolph C,
      4. et al
      . Effects of a symptom-free waiting period on clinical outcome and risk of reinjury after sport-related concussion. Neurosurgery 2009;65:876–82; discussion 882–73.
      OpenUrlCrossRefPubMedWeb of Science
      1. Register-Mihalik J,
      2. Guskiewicz KM,
      3. Mann JD,
      4. et al
      . The effects of headache on clinical measures of neurocognitive function. Clin J Sport Med 2007;17:282–8.
      OpenUrlCrossRefPubMedWeb of Science
      1. Hynes LM,
      2. Dickey JP
      . Is there a relationship between whiplash-associated disorders and concussion in hockey? A preliminary study. Brain Inj 2006;20:179–88.
      OpenUrlCrossRefPubMedWeb of Science
      1. Bruce JM,
      2. Echemendia RJ
      . Concussion history predicts self-reported symptoms before and following a concussive event. Neurology 2004;63:1516–18.
      OpenUrlCrossRef
      1. Field M,
      2. Collins MW,
      3. Lovell MR,
      4. et al
      . Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J Pediatr 2003;142:546–53.
      OpenUrlCrossRefPubMedWeb of Science
      1. Piland SG,
      2. Motl RW,
      3. Ferrara MS,
      4. et al
      . Evidence for the factorial and construct validity of a self-report concussion symptoms scale. J Athl Train 2003;38:104–12.
      OpenUrlPubMed
      1. Johnson PD,
      2. Hertel J,
      3. Olmsted LC,
      4. et al
      . Effect of mild brain injury on an instrumented agility task. Clin J Sport Med 2002;12:12–17.
      OpenUrlCrossRefPubMedWeb of Science
      1. Echemendia RJ,
      2. Putukian M,
      3. Mackin RS,
      4. et al
      . Neuropsychological test performance prior to and following sports-related mild traumatic brain injury. Clin J Sport Med 2001;11:23–31.
      OpenUrlCrossRefPubMedWeb of Science
    54. ↵
      1. McLeod TC Valovich,
      2. Bay RC,
      3. Lam KC,
      4. et al
      . Representative baseline values on the Sport Concussion Assessment Tool 2 (SCAT2) in adolescent athletes vary by gender, grade, and concussion history. Am J Sports Med 2012;40:927–33.
      OpenUrlAbstract/FREE Full Text
    55. ↵
      1. Jinguji TM,
      2. Bompadre V,
      3. Harmon KG,
      4. et al
      . Sport Concussion Assessment Tool-2: baseline values for high school athletes. Br J Sports Med 2012;46:365–70.
      OpenUrlAbstract/FREE Full Text
      1. Moriarity JM,
      2. Pietrzak RH,
      3. Kutcher JS,
      4. et al
      . Unrecognised ringside concussive injury in amateur boxers. Br J Sports Med 2012;46:1011–15.
      OpenUrlAbstract/FREE Full Text
      1. Echlin PS,
      2. Tator CH,
      3. Cusimano MD,
      4. et al
      . Return to play after an initial or recurrent concussion in a prospective study of physician-observed junior ice hockey concussions: implications for return to play after a concussion. Neurosurg Focus 2010;29:E5.
      OpenUrlPubMed
      1. Makdissi M,
      2. Darby D,
      3. Maruff P,
      4. et al
      . Natural history of concussion in sport: markers of severity and implications for management. Am J Sports Med 2010;38:464–71.
      OpenUrlAbstract/FREE Full Text
      1. Covassin T,
      2. Stearne D,
      3. Elbin R
      . Concussion history and postconcussion neurocognitive performance and symptoms in collegiate athletes. J Athl Train 2008;43:119–24.
      OpenUrlCrossRefPubMedWeb of Science
      1. Moriarity J,
      2. Collie A,
      3. Olson D,
      4. et al
      . A prospective controlled study of cognitive function during an amateur boxing tournament. Neurology 2004; 62:1497–502.
      OpenUrlCrossRef
      1. Bleiberg J,
      2. Cernich AN,
      3. Cameron K,
      4. et al
      . Duration of cognitive impairment after sports concussion. Neurosurgery 2004;54:1073–8.
      OpenUrlCrossRefPubMedWeb of Science
      1. Bruce JM,
      2. Echemendia RJ
      . Delayed-onset deficits in verbal encoding strategies among patients with mild traumatic brain injury. Neuropsychology 2003;17:622–9.
      OpenUrlCrossRefPubMedWeb of Science
      1. Daniel JC,
      2. Nassiri JD,
      3. Wilckens J,
      4. et al
      . The implementation and use of the standardized assessment of concussion at the U.S. Naval Academy. Mil Med 2002;167:873–6.
      OpenUrlPubMed
      1. McCrea M,
      2. Kelly JP,
      3. Randolph C,
      4. et al
      . Immediate neurocognitive effects of concussion. Neurosurgery 2002;50:1032–40.
      OpenUrlCrossRefPubMedWeb of Science
      1. Barr WB,
      2. McCrea M
      . Sensitivity and specificity of standardized neurocognitive testing immediately following sports concussion. J Int Neuropsychol Soc 2001;7:693–702.
      OpenUrlCrossRefPubMedWeb of Science
      1. Macciocchi SN,
      2. Barth JT,
      3. Littlefield L,
      4. et al
      . Multiple concussions and neuropsychological functioning in collegiate football players. J Athl Train 2001;36:303–6.
      OpenUrlPubMedWeb of Science
      1. McCrea M
      . Standardized mental status testing on the sideline after sport-related concussion. J Athl Train 2001;36:274–9.
      OpenUrlPubMedWeb of Science
      1. Warden DL,
      2. Bleiberg J,
      3. Cameron KL,
      4. et al
      . Persistent prolongation of simple reaction time in sports concussion. Neurology 2001;57:524–6.
      OpenUrlCrossRef
      1. Collins MW,
      2. Grindel SH,
      3. Lovell MR,
      4. et al
      . Relationship between concussion and neuropsychological performance in college football players. JAMA 1999;282:964–70.
      OpenUrlCrossRefPubMedWeb of Science
      1. McCrea M,
      2. Kelly JP,
      3. Randolph C,
      4. et al
      . Standardized assessment of concussion (SAC): on-site mental status evaluation of the athlete. J Head Trauma Rehabil 1998;13:27–35.
      OpenUrlCrossRefPubMedWeb of Science
      1. McCrea M,
      2. Kelly JP,
      3. Kluge J,
      4. et al
      . Standardized assessment of concussion in football players. Neurology 1997;48:586–8.
      OpenUrlCrossRef
      1. Galetta KM,
      2. Barrett J,
      3. Allen M,
      4. et al
      . The King-Devick test as a determinant of head trauma and concussion in boxers and MMA fighters. Neurology 2011;76:1456–62.
      OpenUrlCrossRef
      1. Galetta KM,
      2. Brandes LE,
      3. Maki K,
      4. et al
      . The King-Devick test and sports-related concussion: study of a rapid visual screening tool in a collegiate cohort. J Neurol Sci 2011;309:34–9.
      OpenUrlCrossRefPubMed
      1. Pearson BC,
      2. Armitage KR,
      3. Horner CW,
      4. et al
      . Saccadometry: the possible application of latency distribution measurement for monitoring concussion. Br J Sports Med 2007;41:610–12.
      OpenUrlAbstract/FREE Full Text

    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

      Files in this Data Supplement:

    Footnotes

    • Contributors MM, GI, RE, MM and MR made substantial contributions to: conception and design, or analysis and interpretation of data; drafting the article or revising it critically for important intellectual content; and final approval of the version to be published. All authors included on a paper fulfil the criteria of authorship. There is no one else who fulfils the criteria but has not been included as an author.

    • Competing interests See the supplementary online data for competing interests (http://dx.doi.org/10.1136/bjsports-2013-092145).

    • Provenance and peer review Commissioned; internally peer reviewed.

    • ▸ References to this paper are available online at http://bjsm.bmjgroup.com