Consensus Statement on Concussion in Sport – the 3rd



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Consensus Statement on Concussion in Sport – the 3rd International Conference on Concussion in Sport held in Zurich, November 2008
Authors:

McCrory P, Meeuwisse W, Johnston K, Dvorak J, Aubry M, Molloy M, Cantu R.



Consensus panelists (listed in alphabetical order): In addition to the authors above, the consensus panellists were Broglio S, Davis G, Dick R, Dvorak J, Echemendia R, Gioia G, Guskiewicz K, Herring S, Iverson G, Kelly J, Kissick J, Makdissi M, McCrea M, Ptito A, Purcell L, Putukian M. Also invited but not in attendance: Bahr R, Engebretsen L, Hamlyn P, Jordan B, Schamasch P.

Corresponding author: A/Prof Paul McCrory

Centre for Health, Exercise & Sports Medicine

University of Melbourne, Parkville, Australia 3010

Tel: +61 3 8344 4135

Fax: +61 3 8344 3771

Email: paulmccr@bigpond.net.au



Word Count: Text: 5523

Tables: 2

References: 148

Pages 40


Competing Interests The authors have no competing interests to declare.

Author affiliations:

P McCrory

Neurologist. Director, Centre for Health, Exercise & Sports Medicine, University of Melbourne, Parkville, Australia 3010



Willem Meeuwisse

Sports Physician, Sport Medicine Centre, Faculty of Kinesiology, and Department of Community Health Sciences, Faculty of Medicine, University of Calgary, 2500 University Drive N.W., Calgary, Alberta, Canada, T2N 1N4



Karen Johnston

Neurosurgeon and Director, Sport Concussion Clinic, Toronto Rehabilitation Institute, 550 University Avenue, Toronto, ON, M5G 2A2 Canada



Jiri Dvorak

Neurologist. Director, FIFA Medical Assessment and Research Center (F-MARC) and Schulthess Clinic, Zurich, Switzerland



Mark Aubry

Chief Medical Officer, International Ice Hockey Federation and Hockey Canada, Co-Director Ottawa Sport Medicine Centre, 1370 Clyde Avenue, Ottawa, Canada, K1T 3Y8



Mick Molloy

Chief Medical Officer, International Rugby Board, Huguenot House, 35-38 St Stephen's Green, Dublin 2, Ireland



Robert Cantu.

Neurosurgeon, 131 ORNAC, Suite 820, John Cuming Building, Emerson Hospital, Concord, MA 01742 USA



Preamble

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 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/or the Sports Concussion Assessment Tool (SCAT2) card and neither is subject to any copyright restriction. The authors request, however that the document and/or 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 concussion


  • Which symptom scale & which sideline assessment tool is best for diagnosis and/or follow up?

  • How extensive should the cognitive assessment be in elite athletes?

  • How extensive should clinical and neuropsychological (NP) testing be at non-elite level?

  • Who should do/interpret the cognitive assessment?

  • Is there a gender difference in concussion incidence and outcomes?


Return to play (RTP) issues

  • Is provocative exercise testing useful in guiding RTP?

  • What is the best RTP strategy for elite athletes?

  • What is the best RTP strategy for non-elite athletes?

  • Is protective equipment (e.g. mouthguards and helmets) useful in reducing concussion incidence and/or severity?


Complex concussion and long term issues

  • Is the Simple versus Complex classification a valid and useful differentiation?

  • Are there specific patient populations at risk of long-term problems?

  • Is there a role for additional tests (e.g. structural and/or functional MR Imaging, balance testing, biomarkers)?

  • Should athletes with persistent symptoms be screened for depression/anxiety?


Paediatric concussion

  • Which symptoms scale is appropriate for this age group?

  • Which tests are useful and how often should baseline testing be performed in this age group?

  • What is the most appropriate RTP guideline for elite and non-elite child and adolescent athlete?


Future directions

  • What is the best method of knowledge transfer and education

  • Is there evidence that new and novel injury prevention strategies work (e.g. changes to rules of the game, fair play strategies etc)?

The Zurich document additionally examines the management issues raised in the previous Prague and Vienna documents and applies the consensus questions to these areas.


Specific research questions and consensus discussion
1) CONCUSSION
1.1 Definition of Concussion

Panel discussion regarding the definition of concussion and its separation from mild traumatic brain injury (mTBI) was held. Although there was acknowledgement 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:


Concussion is defined as a complex pathophysiological process affecting the brain, induced by traumatic 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:

1. Concussion may be caused either by a direct blow to the head, face, neck or elsewhere on the body with an ‘‘impulsive’’ force transmitted to the head.

2. Concussion typically results in the rapid onset of short- lived impairment of neurologic function that resolves spontaneously.

3. Concussion may result in neuropathological changes but the acute clinical symptoms largely reflect a functional disturbance rather than a structural injury.

4. Concussion results in a graded set of clinical symptoms that may or may not involve loss of consciousness. Resolution of the clinical and cognitive symptoms typically follows a sequential course however it is important to note that in a small percentage of cases however, post-concussive symptoms may be prolonged.

5. No abnormality on standard structural neuroimaging studies is seen in concussion.
1.2 Classification of Concussion

There was unanimous agreement to abandon the simple vs. 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 (7-10 day) period, although the recovery time frame may be longer in children and adolescents. (2)


2) CONCUSSION EVALUATION
2.1 Symptoms and signs of acute concussion

The panel agreed that the diagnosis of acute concussion usually involves the assessment of a range of domains including clinical symptoms, physical signs, behavior, 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 pre-participation 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:


  1. Symptoms - somatic (e.g. headache), cognitive (e.g. feeling like in a fog) and/or emotional symptoms (e.g. lability)

  2. Physical signs (e.g. loss of consciousness, amnesia)

  3. Behavioural changes (e.g. irritablity)

  4. Cognitive impairment (e.g. slowed reaction times)

  5. Sleep disturbance (e.g. drowsiness)

If any one or more of these components is present, a concussion should be suspected and the appropriate management strategy instituted.


2.2 On-field or sideline evaluation of acute concussion

When a player shows ANY features of a concussion:





  1. The player should be medically evaluated onsite using standard emergency management principles and particular attention should be given to excluding a cervical spine injury.

  2. The appropriate disposition of the player must be determined by the treating healthcare provider in a timely manner. If no healthcare provider is available, the player should be safely removed from practice or play and urgent referral to a physician arranged.

  3. Once the first aid issues are addressed, then an assessment of the concussive injury should be made using the SCAT2 or other similar tool.

  4. The player should not be left alone following the injury and serial monitoring for deterioration is essential over the initial few hours following injury.

  5. A player with diagnosed concussion should not be allowed to return to play on the day of injury. Occasionally in adult athletes, there may be return to play on the same day as the injury. See section 4.2

It 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 questions (3, 4) and the Standardized Assessment of Concussion (SAC). (5-7) It is worth noting that standard orientation questions (e.g. 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 detect 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.
2.3 Evaluation in emergency room or office by medical personnel

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 encompass:




  1. A medical assessment including a comprehensive history and detailed neurological examination including a thorough assessment of mental status, cognitive functioning and gait and balance.

  2. A determination of the clinical status of the patient including whether there has been improvement or deterioration since the time of injury. This may involve seeking additional information from parents, coaches, teammates and eyewitness to the injury.

  3. A determination of the need for emergent neuroimaging in order to

exclude a more severe brain injury involving a structural abnormality
In large part, these points above are included in the SCAT2 assessment, which forms part of the Zurich consensus statement.
3) CONCUSSION INVESTIGATIONS

A range of additional investigations may be utilized to assist in the diagnosis and/or exclusion of injury. These include:


3.1 Neuroimaging

It was recognized by the panelists that conventional structural neuroimaging is normal in concussive injury. Given that caveat, the following suggestions are made: Brain CT (or where available MR brain scan) contributes little to concussion evaluation but should be employed whenever suspicion of an intra-cerebral structural lesion exists. Examples of such situations may include prolonged disturbance of conscious state, focal neurological deficit or worsening symptoms.


Newer structural MRI modalities including gradient echo, perfusion and diffusion imaging have greater sensitivity for structural abnormalities. However, the lack of published studies as well as absent pre-injury 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 fMRI demonstrate activation patterns that correlate with symptom severity and recovery in concussion. (9-13) Whilst not part of routine assessment at the present time, they nevertheless provide additional insight to pathophysiological mechanisms. Alternative imaging technologies (e.g. 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.
3.2 Objective Balance Assessment

Published studies, using both sophisticated force plate technology, as well as those using less sophisticated clinical balance tests (e.g. 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 where symptoms or signs indicate a balance component. (14-20)


3.3 Neuropsychological Assessment

The 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 case 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 return to play 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 return to play decision should remain a medical one in which a multidisciplinary approach, when possible, has been taken. In the absence of NP and other (e.g. 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 return to play decisions and will not be done until patient is symptom free. (29, 30) There may be situations (e.g. child and adolescent athletes) where testing may be performed early whilst the patient is still symptomatic to assist in determining management. This will normally be best determined in consultation with a trained neuropsychologist. (31, 32)
3.4 Genetic Testing

The 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 demonstrate 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 sporting concussion is not known at this stage. (35-42)


3.5 Experimental Concussion Assessment Modalities

Different electrophysiological recording techniques (e.g. evoked response potential (ERP), cortical magnetic stimulation and electroencephalography) have demonstrated reproducible abnormalities in the post concussive 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 cerebral spinal 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.
4) CONCUSSION MANAGEMENT

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 return to play. 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 injuries will recover spontaneously over several days. In these situations, it is expected that an athlete will proceed progressively through a stepwise return to play 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 (e.g. scholastic work, videogames, 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 re-injury) while symptomatic, no further intervention is required during the period of recovery and the athlete typically resumes sport without further problem.
4.1 Graduated Return to Play Protocol

Return to play protocol following a concussion follows a stepwise process as outlined in Table 1.


Insert table 1 about here
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 one week to proceed through the full rehabilitation protocol once they are asymptomatic at rest and with provocative exercise. If any post concussion 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.
4.2 Same day RTP

With adult athletes, in some settings, where there are team physicians experienced in concussion management and sufficient resources (e.g. access to neuropsychologists, consultants, neuroimaging etc) as well as access to immediate (i.e. sideline) neuro-cognitive assessment, return to play management is may be more rapid. The RTP strategy must still follow the same basic management principles namely, full clinical and cognitive recovery before consideration of return to play.  This approach is supported by published guidelines, such as 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 NFL studies without a risk of recurrence or sequelae. (61) There is data however, demonstrating that at the collegiate and high school level, athletes allowed to RTP on the same day may demonstrate NP deficits post-injury that may not be evident on the sidelines and are more likely to have delayed onset of symptoms. (62-68) It should be emphasised however, the young (<18) elite athlete should be treated more conservatively even though the resources may be the same as an older professional athlete. (See section 6.1)


4.3 Psychological management and mental health issues

In addition, psychological approaches may have potential application in this injury, particularly with the modifiers listed below. (69, 70) Care givers are also encouraged to evaluate the concussed athlete for affective symptoms such as depression as these symptoms may be common in concussed athletes.(57)


4.4 The Role of Pharmacological Therapy

Pharmacological therapy in sports concussion may be applied in two distinct situations. The first of these situations is the management of specific prolonged symptoms (e.g. 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 be only 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 pharmacological agents/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 return to play while still on such medication must be considered carefully by the treating clinician.
4.5 The role of pre-participation concussion evaluation

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 pre-identify athletes that fit into a high risk category and provides an opportunity for the healthcare 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 or cervical spine injuries as these may also have clinical relevance. It is worth emphasizing that in the setting of maxillofacial and cervical spine injuries, co- existent concussive injuries may be missed unless specifically assessed. Questions pertaining to disproportionate impact 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. The benefit a comprehensive pre-participation concussion evaluation allows for modification and optimization of protective behavior and an opportunity for education.

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