Consensus Statement on Concussion in Sport: The 3rd International Conference on Concussion in Sport Held in Zurich, November 2008

Abstract

This paper is a revision and update of the recommendations developed following the 1st (Vienna) and 2nd (Prague) International Symposia on Concussion in Sport.1,2 The Zurich Consensus statement is designed to build on the principles outlined in the original Vienna and Prague documents and to develop further conceptual understanding of this problem using a formal consensus-based approach. A detailed description of the consensus process is outlined at the end of this document under the background section (see Section 11). This document is developed for use by physicians, therapists, certified athletic trainers, health professionals, coaches, and other people involved in the care of injured athletes, whether at the recreational, elite, or professional level.While agreement exists pertaining to principal messages conveyed within this document, the authors acknowledge that the science of concussion is evolving and, therefore, management and return-to-play (RTP) decisions remain in the realm of clinical judgment on an individualized basis. Readers are encouraged to copy and distribute freely the Zurich Consensus document and the Sports Concussion Assessment Tool (SCAT2) card, and neither is subject to any copyright restriction. The authors request, however, that the document and the SCAT2 card be distributed in their full and complete format.The following focus questions formed the foundation for the Zurich concussion consensus statement:Acute Simple ConcussionRTP IssuesComplex Concussion and Long-Term IssuesPediatric ConcussionFuture DirectionsThe Zurich document additionally examines the management issues raised in the previous Prague and Vienna documents and applies the consensus questions to these areas.Panel discussion regarding the definition of concussion and its separation from mild traumatic brain injury (mTBI) was held. Although there was acknowledgment that the terms refer to different injury constructs and should not be used interchangeably, it was not felt that the panel would define mTBI for the purpose of this document. There was unanimous agreement, however, that concussion is defined as follows:There was unanimous agreement to abandon the “simple” versus “complex” terminology that had been proposed in the Prague agreement statement, as the panel felt that the terminology itself did not fully describe the entities. The panel, however, unanimously retained the concept that the majority (80%–90%) of concussions resolve in a short (7- to 10-day) period, although the recovery time frame may be longer in children and adolescents.2The panel agreed that the diagnosis of acute concussion usually involves the assessment of a range of domains, including clinical symptoms, physical signs, behaviour, balance, sleep, and cognition. Furthermore, a detailed concussion history is an important part of the evaluation, both in the injured athlete and when conducting a preparticipation examination. The detailed clinical assessment of concussion is outlined in the SCAT2 form, which is an appendix to this document.The suspected diagnosis of concussion can include one or more of the following clinical domains:If any one or more of these components is present, a concussion should be suspected and the appropriate management strategy instituted.When a player shows ANY features of a concussionIt was unanimously agreed that sufficient time for assessment and adequate facilities should be provided for the appropriate medical assessment, both on and off the field, for all injured athletes. In some sports, this may require rule change to allow an off-field medical assessment to occur without affecting the flow of the game or unduly penalizing the injured player's team.Sideline evaluation of cognitive function is an essential component in the assessment of this injury. Brief neuropsychological test batteries that assess attention and memory function have been shown to be practical and effective. Such tests include the Maddocks questions3,4 and the Standardized Assessment of Concussion (SAC).5–7 It is worth noting that standard orientation questions (eg, time, place, person) have been shown to be unreliable in the sporting situation when compared with memory assessment.4,8 It is recognized, however, that abbreviated testing paradigms are designed for rapid concussion screening on the sidelines and are not meant to replace comprehensive neuropsychological testing, which is sensitive to detecting subtle deficits that may exist beyond the acute episode, nor should they be used as a stand-alone tool for the ongoing management of sports concussions.It should also be recognized that the appearance of symptoms might be delayed several hours following a concussive episode.An athlete with concussion may be evaluated in the emergency room or doctor's office as a point of first contact following injury or may have been referred from another care provider. In addition to the points outlined above, the key features of this exam should encompassIn large part, the points above are included in the SCAT2 assessment, which is included in the Zurich consensus statement.A range of additional investigations may be utilized to assist in the diagnosis and/or exclusion of injury. These include the following.It was recognized by the panelists that conventional structural neuroimaging is normal in concussive injury. Given that caveat, the following suggestions are made: Brain computed tomography (CT) (or, where available, MR brain scan) contributes little to concussion evaluation but should be employed whenever suspicion of an intracerebral structural lesion exists. Examples of such situations may include prolonged disturbance of conscious state, focal neurologic deficit, or worsening symptoms.Newer structural MR imaging modalities, including gradient echo, perfusion, and diffusion imaging, have greater sensitivity for structural abnormalities. However, the lack of published studies as well as absent preinjury neuroimaging data limits the usefulness of this approach in clinical management at the present time. In addition, the predictive value of various MR abnormalities that may be incidentally discovered is not established at the present time.Other imaging modalities such as functional magnetic resonance imaging (fMRI) demonstrate activation patterns that correlate with symptom severity and recovery in concussion.9–13 While not part of routine assessment at the present time, they nevertheless provide additional insight to pathophysiologic mechanisms. Alternative imaging technologies (eg, positron emission tomography, diffusion tensor imaging, magnetic resonance spectroscopy, functional connectivity), while demonstrating some compelling findings, are still at early stages of development and cannot be recommended other than in a research setting.Published studies using both sophisticated force plate technology as well as those using less sophisticated clinical balance tests (eg, Balance Error Scoring System [BESS]) have identified postural stability deficits lasting approximately 72 hours following sport-related concussion. It appears that postural stability testing provides a useful tool for objectively assessing the motor domain of neurologic functioning and should be considered a reliable and valid addition to the assessment of athletes suffering from concussion, particularly when symptoms or signs indicate a balance component.14–20The application of neuropsychological (NP) testing in concussion has been shown to be of clinical value and continues to contribute significant information in concussion evaluation.21–26 Although in most cases cognitive recovery largely overlaps with the time course of symptom recovery, it has been demonstrated that cognitive recovery may occasionally precede or more commonly follow clinical symptom resolution, suggesting that the assessment of cognitive function should be an important component in any RTP protocol.27,28 It must be emphasized, however, that NP assessment should not be the sole basis of management decisions; rather, it should be seen as an aid to the clinical decision-making process in conjunction with a range of clinical domains and investigational results.Neuropsychologists are in the best position to interpret NP tests by virtue of their background and training. However, there may be situations where neuropsychologists are not available and other medical professionals may perform or interpret NP screening tests. The ultimate RTP decision should remain a medical one, in which a multidisciplinary approach, when possible, has been taken. In the absence of NP and other (eg, formal balance assessment) testing, a more conservative return-to-play approach may be appropriate.In the majority of cases, NP testing will be used to assist RTP decisions and will not be done until the patient is symptom free.29,30 There may be persons (eg, child and adolescent athletes) in whom testing may be performed early while the patient is still symptomatic to assist in determining management. This will normally be best determined in consultation with a trained neuropsychologist.31,32The significance of apolipoprotein (Apo) E4, ApoE promotor gene, tau polymerase, and other genetic markers in the management of sports concussion risk or injury outcome is unclear at this time.33,34 Evidence from human and animal studies in more severe traumatic brain injury demonstrates induction of a variety of genetic and cytokine factors, such as insulin-like growth factor-1 (IGF-1), IGF binding protein-2, fibroblast growth factor, Cu-Zn superoxide dismutase, superoxide dismutase-1 (SOD-1), nerve growth factor, glial fibrillary acidic protein (GFAP), and S-100. Whether such factors are affected in sport concussion is not known at this stage.35–42Different electrophysiologic recording techniques (eg, evoked response potential [ERP], cortical magnetic stimulation, and electroencephalography) have demonstrated reproducible abnormalities in the postconcussive state. However, not all studies reliably differentiated concussed athletes from controls.43–49 The clinical significance of these changes remains to be established.In addition, biochemical serum and cerebrospinal fluid markers of brain injury (including S-100, neuron specific enolase [NSE], myelin basic protein [MBP], GFAP, tau, etc) have been proposed as means by which cellular damage may be detected if present.50–56 There is currently insufficient evidence, however, to justify the routine use of these biomarkers clinically.The cornerstone of concussion management is physical and cognitive rest until symptoms resolve and then a graded program of exertion prior to medical clearance and RTP. The recovery and outcome of this injury may be modified by a number of factors that may require more sophisticated management strategies. These are outlined in the section on modifiers below.As described above, the majority of patients will recover spontaneously over several days. In these situations, it is expected that an athlete will proceed progressively through a stepwise RTP strategy.57 During this period of recovery while symptomatic following an injury, it is important to emphasize to the athlete that physical AND cognitive rest is required. Activities that require concentration and attention (eg, scholastic work, video games, text messaging, etc) may exacerbate symptoms and possibly delay recovery. In such cases, apart from limiting relevant physical and cognitive activities (and other risk-taking opportunities for reinjury) while symptomatic, no further intervention is required during the period of recovery, and the athlete typically resumes sport without further problem.Return-to-play protocol following a concussion follows a stepwise process as outlined in Table 1.With this stepwise progression, the athlete should continue to proceed to the next level if asymptomatic at the current level. Generally each step should take 24 hours, so that an athlete would take approximately 1 week to proceed through the full rehabilitation protocol once asymptomatic at rest and with provocative exercise. If any postconcussion symptoms occur while in the stepwise program, then the patient should drop back to the previous asymptomatic level and try to progress again after a further 24-hour period of rest has passed.With adult athletes, in some settings, where there are team physicians experienced in concussion management and sufficient resources (eg, access to neuropsychologists, consultants, neuroimaging, etc) as well as access to immediate (ie, sideline) neurocognitive assessment, RTP management may be more rapid. The RTP strategy must still follow the same basic management principles: namely, full clinical and cognitive recovery before consideration of RTP. This approach is supported by published guidelines, such as those from the American Academy of Neurology, US Team Physician Consensus Statement, and US National Athletic Trainers' Association position statement.58–60 This issue was extensively discussed by the consensus panelists, and it was acknowledged that there is evidence that some professional American football players are able to RTP more quickly, with even same-day RTP supported by National Football League studies without a risk of recurrence or sequelae.61 There are data, however, demonstrating that at the collegiate and high school levels, athletes allowed to RTP on the same day may demonstrate NP deficits postinjury that may not be evident on the sidelines and are more likely to have delayed onset of symptoms.62–68 Yet it should be emphasized that the young (less than 18 years old) elite athlete should be treated more conservatively, even though the resources may be the same as for an older professional athlete (see section 6.1).In addition, psychological approaches may have potential application in this injury, particularly with the modifiers listed below.69,70 Caregivers are also encouraged to evaluate the concussed athlete for affective symptoms, such as depression, as these symptoms may be common in concussed athletes.57Pharmacologic therapy in sports concussion may be applied in 2 distinct situations. The first of these situations is the management of specific, prolonged symptoms (eg, sleep disturbance, anxiety, etc). The second situation is where drug therapy is used to modify the underlying pathophysiology of the condition with the aim of shortening the duration of the concussion symptoms.71 In broad terms, this approach to management should only be considered by clinicians experienced in concussion management.An important consideration in RTP is that concussed athletes should not only be symptom free but also should not be taking any pharmacologic agents or medications that may mask or modify the symptoms of concussion. Where antidepressant therapy may be commenced during the management of a concussion, the decision to RTP while still on such medication must be considered carefully by the treating clinician.Recognizing the importance of a concussion history and appreciating the fact that many athletes will not recognize all the concussions they may have suffered in the past, a detailed concussion history is of value.72–75 Such a history may identify early those athletes who fit into a high-risk category and provides an opportunity for the health care provider to educate the athlete in regard to the significance of concussive injury. A structured concussion history should include specific questions as to previous symptoms of a concussion, not just the perceived number of past concussions. It is also worth noting that dependence upon the recall of concussive injuries by teammates or coaches has been demonstrated to be unreliable.72 The clinical history should also include information about all previous head, face, and cervical spine injuries, as these may also have clinical relevance. It is worth emphasizing that in the setting of maxillofacial and cervical spine injuries, coexistent concussive injuries may be missed unless specifically assessed. Questions pertaining to disproportionate impact versus symptom severity may alert the clinician to a progressively increasing vulnerability to injury. As part of the clinical history, it is advised that details regarding protective equipment employed at time of injury be sought, both for recent and remote injuries. A comprehensive preparticipation concussion evaluation allows for modification and optimization of protective behaviour and an opportunity for education.The consensus panel agreed that a range of “modifying” factors may influence the investigation and management of concussion and, in some cases, may predict the potential for prolonged or persistent symptoms. These modifiers would also be important to consider in a detailed concussion history and are outlined in Table 2.In this setting, there may be additional management considerations beyond simple RTP advice. There may be a more important role for additional investigations including formal NP testing, balance assessment, and neuroimaging. It is envisioned that athletes with such modifying features would be managed in a multidisciplinary manner coordinated by a physician with specific expertise in the management of concussive injury.The role of female gender as a possible modifier in the management of concussion was discussed at length by the panel. There was not unanimous agreement that the current published research evidence is conclusive that this should be included as a modifying factor, although it was accepted that sex may be a risk factor for injury and/or influence injury severity.76–78In the overall management of moderate to severe traumatic brain injury, duration of loss of consciousness (LOC) is an acknowledged predictor of outcome.79 While published findings in concussion describe LOC associated with specific early cognitive deficits, it has not been noted as a measure of injury severity.80,81 Consensus discussion determined that prolonged (greater than 1 minute in duration) LOC would be considered as a factor that may modify management.There is renewed interest in the role of posttraumatic amnesia and its role as a surrogate measure of injury severity.67,82,83 Published evidence suggests that the nature, burden, and duration of the clinical postconcussive symptoms may be more important than the presence or duration of amnesia alone.80,84,85 Further, it must be noted that retrograde amnesia varies with the time of measurement postinjury and, hence, is poorly reflective of injury severity.86,87A variety of immediate motor phenomena (eg, tonic posturing) or convulsive movements may accompany a concussion. Although dramatic, these clinical features are generally benign and require no specific management beyond the standard treatment of the underlying concussive injury.88,89Mental health issues (such as depression) have been reported as a long-term consequences of traumatic brain injury, including sports-related concussion. Neuroimaging studies using fMRI suggest that a depressed mood following concussion may reflect an underlying pathophysiologic abnormality consistent with a limbic-frontal model of depression.52,90–100There was unanimous agreement by the panel that the evaluation and management recommendations contained herein could be applied to children and adolescents down to the age of 10 years. Below that age, children report different concussion symptoms from adults and would require age-appropriate symptom checklists as a component of assessment. An additional consideration in assessing the child or adolescent athlete with a concussion is that in the clinical evaluation by the health care professional, there may be the need to include both patient and parental input, as well as teacher and school input, when appropriate.101–107The decision to use NP testing is broadly the same as in the adult assessment paradigm. However, timing of testing may differ in order to assist planning in school and home management (and may be performed while the patient is still symptomatic). If cognitive testing is performed, then it must be developmentally sensitive until the late teen years, due to the ongoing cognitive maturation that occurs during this period, which, in turn, makes the utility of comparison to either the person's own baseline performance or to population norms limited.20 In this age group, it is more important to consider the use of trained neuropsychologists to interpret assessment data, particularly in children with learning disorders and/or attention deficit hyperactivity disorder (ADHD), who may need more sophisticated assessment strategies.31,32,101The panel strongly endorsed the view that children should not be returned to practice or play until clinically completely symptom free, which may require a longer time frame than for adults. In addition, the concept of “cognitive rest” was highlighted, with special reference to a child's need to limit exertion with activities of daily living and to limit scholastic and other cognitive stressors (eg, text messaging, video games, etc) while symptomatic. School attendance and activities may also need to be modified to avoid provocation of symptoms.Because of the different physiological response and longer recovery after concussion and specific risks (eg, diffuse cerebral swelling) related to head impact during childhood and adolescence, a more conservative RTP approach is recommended. It is appropriate to extend the amount of time of asymptomatic rest and/or the length of the graded exertion in children and adolescents. It is not appropriate for a child or adolescent athlete with concussion to RTP on the same day as the injury, regardless of the level of athletic performance. Concussion modifiers apply even more to this population than to adults and may mandate more cautious RTP advice.The panel unanimously agreed that all athletes, regardless of level of participation, should be managed using the same treatment and RTP paradigm. A more useful construct was agreed to, whereby the available resources and expertise in concussion evaluation were of more importance in determining management than a separation between elite and non-elite athlete management. Although formal baseline NP screening may be beyond the resources of many sports or individuals, it is recommended that in all organized high-risk sports, consideration be given to having this cognitive evaluation, regardless of the age or level of performance.Epidemiologic studies have suggested an association between repeated sports concussions during a career and late-life cognitive impairment. Similarly, case reports have noted anecdotal cases in which neuropathologic evidence of chronic traumatic encephalopathy was observed in retired football players.108–112 Panel discussion was held, and no consensus was reached on the significance of such observations at this stage. Clinicians need to be mindful of the potential for long-term problems in the management of all athletes.There is no good clinical evidence that currently available protective equipment will prevent concussion, although mouthguards have a definite role in preventing dental and orofacial injury. Biomechanical studies have shown a reduction in impact forces to the brain with the use of head gear and helmets, but these findings have not been translated to show a reduction in concussion incidence. For skiing and snowboarding, there are a number of studies to suggest that helmets provide protection against head and facial injury and, hence, should be recommended for participants in alpine sports.113–116 In specific sports such as cycling, motor, and equestrian sports, protective helmets may prevent other forms of head injury (eg, skull fracture) that are related to falling on hard road surfaces, and these may be an important injury prevention issue for those sports.116–128Consideration of rule changes to reduce the head injury incidence or severity may be appropriate where a clear-cut mechanism is implicated in a particular sport. An example of this is in football (soccer), in which research studies demonstrated that upper limb-to-head contact in heading contests accounted for approximately 50% of concussions.129 As noted earlier, rule changes also may be needed in some sports to allow an effective off-field medical assessment to occur without compromising the athlete's welfare, affecting the flow of the game, or unduly penalizing the player's team. It is important to note that rule enforcement may be a critical aspect of modifying injury risk in these settings, and referees play an important role in this regard.An important consideration in the use of protective equipment is the concept of risk compensation.130 This is where the use of protective equipment results in behavioural change, such as the adoption of more dangerous playing techniques, which can result in a paradoxical increase in injury rates. This may be a particular concern in child and adolescent athletes, in whom head injury rates are often higher than in adult athletes.131–133The competitive/aggressive nature of sport that makes it fun to play and watch should not be discouraged. However, sporting organizations should be encouraged to address violence that may increase concussion risk.134,135 Fair play and respect should be supported as key elements of sport.As the ability to treat or reduce the effects of concussive injury after the event is minimal, education of athletes, colleagues, and the general public is a mainstay of progress in this field. Athletes, referees, administrators, parents, coaches, and health care providers must be educated regarding the detection of concussion, its clinical features, assessment techniques, and principles of safe RTP. Methods to improve education, including Web-based resources, educational videos, and international outreach programs, are important in delivering the message. In addition, concussion working groups plus the support and endorsement of enlightened sport groups such as Fédération Internationale de Football Association (FIFA), International Olympic Commission (IOC), International Rugby Board (IRB), and International Ice Hockey Federation (IIHF), who initiated this endeavor, have enormous value and must be pursued vigorously. Fair play and respect for opponents are ethical values that should be encouraged in all sports and sporting associations. Similarly coaches, parents, and managers play an important part in ensuring these values are implemented on the field of play.57,136–148The consensus panelists recognize that research is needed across a range of areas in order to answer some critical research questions. The key areas for research identified includeThis consensus document reflects the current state of knowledge and will need to be modified according to the development of new knowledge. It provides an overview of issues that may be of importance to health care providers involved in the management of sports-related concussion. It is not intended as a standard of care and should not be interpreted as such. This document is only a guide, and is of a general nature, consistent with the reasonable practice of a health care professional. Individual treatment will depend on the facts and circumstances specific to each individual case.It is intended that this document will be formally reviewed and updated prior to December 1, 2012.In November 2001, the 1st International Conference on Concussion in Sport was held in Vienna, Austria. This meeting was organized by the IIHF in partnership with FIFA and the Medical Commission of the IOC. As part of the resulting mandate for the future, the need for leadership and future updates was identified. The 2nd International Conference on Concussion in Sport was organized by the same group, with the additional involvement of the IRB, and was held in Prague, Czech Republic, in November 2004. The original aims of the symposia were to provide recommendations for the improvement of safety and health of athletes who suffer concussive injuries in ice hockey, rugby, football (soccer), and other sports. To this end, a range of experts were invited to both meetings to address specific issues of epidemiology, basic and clinical science, injury grading systems, cognitive assessment, new research methods, protective equipment, management, prevention, and long-term outcome.1,2The 3rd International Conference on Concussion in Sport was held in Zurich, Switzerland, on October 29–30, 2008, and was designed as a formal consensus meeting following the organizational guidelines set forth by the US National Institutes of Health. (Details of the consensus methodology can be obtained at: http://consensus.nih.gov/ABOUTCDP.htm.) The basic principles governing the conduct of a consensus development conference are summarized below:The panel chairperson (W.M.) did not identify with any advocacy position. The chairperson was responsible for directing the consensus session and guiding the panel's deliberations. Panelists were drawn from clinical practice, academics, and research in the field of sports-related concussion. They do not represent organizations per se but were selected for their expertise, experience, and understanding of this field.