Abstract

This paper is a revision and update of the recommendations developed following the 1st (Vienna 2001), 2nd (Prague 2004), and 3rd (Zurich 2008) International Consensus Conference on Concussion in Sport and is based on the deliberations at the 4th International Conference on Concussion in Sport held in Zurich, November 2012.1–3The new 2012 Zurich Consensus statement is designed to build on the principles outlined in the previous 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. This document is developed for use by physicians and health care professionals who are primarily involved in the care of injured athletes, whether at the recreational, elite, or professional level.While agreement exists pertaining to principle messages conveyed within this document, the authors acknowledge that the science of concussion is evolving, and therefore, management and 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, the Pocket Concussion Recognition Tool (CRT), the Sports Concussion Assessment Tool version 3 (SCAT3), and the Child SCAT3 card (Appendix), and none is subject to any restriction, provided it is not altered in any way or converted to a digital format. The authors request that the document and the accompanying tools be distributed in their full and complete format.This consensus paper is broken into a number of sections:The Zurich 2012 document examines sport concussion and management issues raised in the previous Vienna 2001, Prague 2004, and Zurich 2008 documents and applies the consensus questions from Section 3 to these areas.1–3Panel discussion regarding the definition of concussion and its separation from mild traumatic brain injury (mTBI) was held. There was acknowledgement by the Concussion in Sport Group (CISG) that, although the terms mild traumatic brain injury (mTBI) and concussion are often used interchangeably in the sporting context and particularly in the US literature, others use the term to refer to different injury constructs. Concussion is the historical term representing low-velocity injuries that cause brain “shaking,” resulting in clinical symptoms, and which are not necessarily related to a pathologic injury. Concussion is a subset of TBI, and the term concussion will be used in this document. It was also noted that the term commotio cerebri is often used in European and other countries. Minor revisions were made to the definition of concussion and it is defined as follows: Concussion is a brain injury and is defined as a complex pathophysiological process affecting the brain, induced by biomechanical forces. Several common features that incorporate clinical, pathologic, and biomechanical injury constructs that may be utilized in defining the nature of a concussive head injury include:The majority (80% to 90%) of concussions resolve in a short (7–10 day) period, although the recovery timeframe may be longer in children and adolescents.2The diagnosis of acute concussion usually involves the assessment of a range of domains including clinical symptoms, physical signs, cognitive impairment, neurobehavioral features, and sleep disturbance. 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 SCAT3 and Child SCAT3 forms, which are appendices to this document.The suspected diagnosis of concussion can include 1 or more of the following clinical domains:If any 1 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 concussion: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 appropriate off-field medical assessment to occur without affecting the flow of the game or unduly penalizing the injured player's team. The final determination regarding concussion diagnosis and fitness to play is a medical decision based on clinical judgment.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 SCAT3, which incorporates the Maddocks questions,4,5 and the Standardized Assessment of Concussion (SAC).6–8 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.5,9 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 should ideally be performed by trained neuropsychologists who are sensitive to subtle deficits that may exist beyond the acute episode; nor should they be used as a standalone tool for the ongoing management of sports concussions.It should also be recognized that the appearance of symptoms or cognitive deficit might be delayed several hours after a concussive episode and that concussion should be seen as an evolving injury in the acute stage.An athlete with concussion may be evaluated in the emergency room or doctor's office as a point of first contact after injury or may have been referred from another care provider. In addition to the points outlined above, the key features of this exam should encompass:In large part, the points above are included in the SCAT3 assessment.A range of additional investigations may be used to assist in the diagnosis or exclusion of injury. Conventional structural neuroimaging is typically normal in concussive injury. Given that caveat, the following suggestions are made. Brain computed tomography (CT; or where available, magnetic resonance imaging [MRI]) contributes little to concussion evaluation but should be employed whenever suspicion of an intracerebral or structural lesion (eg, skull fracture) exists. Examples of such situations may include prolonged disturbance of conscious state, focal neurological deficit, or worsening symptoms.Other imaging modalities, such as functional MRI (fMRI) demonstrate activation patterns that correlate with symptom severity and recovery in concussion.10–14 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), have identified acute postural stability deficits lasting approximately 72 hours after 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 where symptoms or signs indicate a balance component.15–21The 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.22,23 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. How such factors are affected in sporting concussion is not known at this stage.24–31 In addition, biochemical serum and cerebrospinal fluid biomarkers 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.32–38 There is currently insufficient evidence, however, to justify the routine use of these biomarkers clinically.Different electrophysiologic recording techniques (eg, evoked response potential, cortical magnetic stimulation, and electroencephalography) have demonstrated reproducible abnormalities in the postconcussive state; however, not all studies reliably differentiated concussed athletes from controls.39–45 The clinical significance of these changes remains to be established.The application of neuropsychological (NP) testing in concussion has been shown to be of clinical value and contributes significant information in concussion evaluation.46–51 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 the overall assessment of concussion and, in particular, any RTP protocol.52,53 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 assessments of different clinical domains and investigational results.It is recommended that all athletes should have a clinical neurological assessment (including assessment of their cognitive function) as part of their overall management. This will normally be done by the treating physician, often in conjunction with computerized NP screening tools.Formal NP testing is not required for all athletes; however, when this is considered necessary, then it should ideally be performed by a trained neuropsychologist. Although neuropsychologists are in the best position to interpret NP tests by virtue of their background and training, 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 RTP approach may be appropriate.Neuropsychological testing may be used to assist RTP decisions and is typically performed when an athlete is clinically asymptomatic. However, NP assessment may add important information in the early stages after injury.54,55 There may be particular situations where testing is performed early to assist in determining aspects of management (eg, return to school in a pediatric athlete). This will normally be best determined in consultation with a trained neuropsychologist.56,57Baseline NP testing was considered by the panel and was not felt to be required as a mandatory aspect of every assessment. However, it may be helpful or add useful information to the overall interpretation of these tests. It also provides an additional educative opportunity for the physician to discuss the significance of this injury with the athlete. At present, there is insufficient evidence to recommend the widespread routine use of baseline NP testing.The cornerstone of concussion management is physical and cognitive rest until the acute symptoms resolve and then a graded program of exertion before medical clearance and RTP. The current published evidence evaluating the effect of rest after a sport-related concussion is sparse. An initial period of rest in the acute symptomatic period after injury (24–48 hours) may be of benefit. Further research to evaluate the long-term outcome of rest and the optimal amount and type of rest is needed. In the absence of evidence-based recommendations, a sensible approach involves the gradual return to school and social activities (before contact sports) in a manner that does not result in a significant exacerbation of symptoms.Low-level exercise for those who are slow to recover may be of benefit, although the optimal timing after injury for initiation of this treatment is currently unknown.As described above, the majority of injuries will recover spontaneously over several days. In these situations, it is expected that an athlete will proceed progressively through a stepwise RTP strategy.58The RTP protocol after 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.It was unanimously agreed that no RTP on the day of concussive injury should occur. There are data demonstrating that, at the collegiate and high school level, 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.59–65Persistent symptoms (>10 days) are reported in 10%–15% of concussions. In general, symptoms are not specific to concussion, and it is important to consider other conditions. Cases of concussion in sport where clinical recovery falls outside the expected window (ie, 10 days) should be managed in a multidisciplinary manner by health care providers with experience in sports-related concussion.Psychological approaches may have potential application in this injury, particularly with the modifiers listed below.66,67 Physicians are also encouraged to evaluate the concussed athlete for affective symptoms such as depression and anxiety, as these symptoms are common in all forms of traumatic brain injury.58Pharmacologic therapy in sports concussion may be applied in 2 distinct situations. The first of these situations is the management of specific or prolonged symptoms (eg, sleep disturbance, anxiety). 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.68 In broad terms, this approach to management should be considered only 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.69–72 Such a history may pre-identify 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 and length of recovery, 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.69 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 effect versus symptom-severity matching 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.There is an additional and often unrecognized benefit of the preparticipation physical examination insofar as the evaluation allows for an educative opportunity with the player concerned as well as consideration of modification of playing behavior if required.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. However, in some cases, the evidence for their efficacy is limited. These modifiers would be important to consider in a detailed concussion history and are outlined in Table 2.The role of female sex 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 enough for this to be included as a modifying factor, although it was accepted that sex may be a risk factor for injury or influence injury severity (or both).73–75In the overall management of moderate to severe traumatic brain injury, duration of loss of consciousness (LOC) is an acknowledged predictor of outcome.76 While published findings in concussion describe LOC associated with specific early cognitive deficits, it has not been noted as a measure of injury severity.77,78 Consensus discussion determined that prolonged (>1-minute 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.64,79,80 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.77,81,82 Further, it must be noted that retrograde amnesia varies with the time of measurement postinjury and hence is poorly reflective of injury severity.83,84A 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.85,86Mental health issues (such as depression) have been reported as a consequence of all levels of traumatic brain injury, including sports-related concussion. Neuroimaging studies using fMRI suggest that a depressed mood after concussion may reflect an underlying pathophysiological abnormality consistent with a limbic-frontal model of depression.34,87–97 While such mental health issues may be multifactorial in nature, it is recommended that the treating physician consider these issues in the management of concussed patients.The evaluation and management recommendations contained herein can be applied to children and adolescents down to the age of 13 years. Below that age, children report concussion symptoms different 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 the clinical evaluation by the health care professional may need to include both patient and parent input and possibly teacher and school input when appropriate.98–104 A child SCAT3 has been developed to assess concussion (see Appendix) for those aged 5–12 years.The decision to use NP testing is broadly the same as the adult assessment paradigm, although there are some differences. Timing of testing may differ in order to assist planning in school and home management. If cognitive testing is performed, then it must be developmentally sensitive until 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 pediatric neuropsychologists to interpret assessment data, particularly in children with learning disorders or attention-deficit hyperactivity disorder, who may need more sophisticated assessment strategies.56,57,98It was agreed by the panel that no return to sport or activity should occur before the child or adolescent athlete has managed to return to school successfully. 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 that may exacerbate symptoms. School attendance and activities may also need to be modified to avoid provocation of symptoms. Children should not be returned to sport until clinically completely symptom free, which may require a longer timeframe than for adults.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 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 adults and may mandate more cautious RTP advice.All athletes, regardless of level of participation, should be managed using the same treatment and RTP paradigm. The available resources and expertise in concussion evaluation are of more importance in determining management than a separation between elite and nonelite athlete management. Although formal NP testing 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.Clinicians need to be mindful of the potential for long-term problems in the management of all athletes. However, it was agreed that chronic traumatic encephalopathy (CTE) represents a distinct tauopathy with an unknown incidence in athletic populations. It was further agreed that a cause-and-effect relationship has not yet been demonstrated between CTE and concussions or exposure to contact sports.105–114 At present, the interpretation of causation in the modern CTE case studies should proceed cautiously. It was also recognized that it is important to address the fears of parents and athletes from media pressure related to the possibility of CTE.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.115–118 In specific sports, such as cycling and motor and equestrian sports, protective helmets may prevent other forms of head injury (eg, skull fracture) that are related to falling on hard surfaces and may be an important injury-prevention issue for those sports.118–130Consideration 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), where research studies demonstrated that upper limb-to-head contact in heading contests accounted for approximately 50% of concussions.131 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.132 This is where the use of protective equipment results in behavioral change such as the adoption of more dangerous playing techniques, which can result in a paradoxical increase in injury rates. The degree to which this phenomenon occurs is discussed in more detail in the review published in the British Journal of Sports Medicine supplement. This may be a particular concern in child and adolescent athletes, in whom head injury rates are often higher than in adult athletes.133–135The 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.136,137 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 the Fédération Internationale de Football Association (FIFA), International Olympic Commission (IOC), International Rugby Board (IRB), and International Ice Hockey Federation (IIHF) that 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.58,138–150In 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 were 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, and football (soccer), as well as 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 29–30 October 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.H.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.The 4th International Conference on Concussion in Sport was held in Zurich, Switzerland, on 1–3 November 2012 and followed the same outline as for the 3rd meeting. All speakers, consensus panel members, and abstract authors were required to sign an International Committee of Medical Journal Editors Form for Disclosure of Potential Conflicts of Interest. Detailed information related to each author's affiliations and conflicts of interests will be made publicly available on the Concussion in Sport Group Web site and published with the British Journal of Sports Medicine supplement.This 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