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Clinical Journal of Sport Medicine:
doi: 10.1097/JSM.0b013e3181b2c114
Editorial

Concussion Consensus: Raising the Bar and Filling in the Gaps

McKeag, Douglas B MD, MS*; Kutcher, Jeffrey S MD†

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From *Indiana University School of Medicine, Department of Family Medicine, Robert Long Hospital, Indianapolis, Indiana; and †Department of Neurology, University of Michigan Medical School, Ann Arbor, Michigan.

Reprints: Douglas B. McKeag, MD, MS, OneAmerica Professor and Chair, Indiana University School of Medicine, Department of Family Medicine, Robert Long Hospital, Second Floor, 1110 West Michigan St, Indianapolis, IN 46202-5102 (e-mail: dmckeag@iupui.edu).

The 3rd International Consensus Statement on Concussion in Sport was published in last month's issue of CJSM; it was the product of a meeting held in Zurich, Switzerland, in October 2008.1 This meeting and the resulting publication were intended to build on the consensus statements produced from international conferences held in Vienna (2002) and Prague (2005).2,3 The organizers of the Zurich conference used the formalized consensus-building process described by the US National Institutes of Health.4

The outcome of the Zurich meeting represents another significant step forward in our understanding and approaches to the management of sports-related concussion. We support the consensus position that the classification of concussion into “simple” versus “complex” be abandoned. The collective clinical experience of sports medicine points to little practical value in making this distinction. We agree that in some sports, such as soccer and rugby, there exists a significant obstacle to providing appropriate medical care as the result of rules that do not allow for stoppage in play and timely evaluation of injured athletes on the field. We are pleased to see the concept of “special populations” reinforced, with recognition of the unique qualities of the pediatric population being especially noteworthy.

Consensus statements, by their nature, suffer from a common malady: They are frequently products of compromise. They may reflect the “average” or agreed-upon thinking on a subject.5 As much as we would like such statements to be evidence based, they often wander into experiential thought and anecdote. Frequently, clinically relevant issues are not discussed at all because of a lack of background science, and if they are, the group's “best guess” becomes consensus. Often, these factors combine to create a very real gap between a consensus statement and its true clinical applicability.6 Although we celebrate the achievement of the 3rd International Consensus Statement on Concussion in Sport, we wish to take this opportunity one step further. What follows is a discussion that not only highlights what we feel are the important ‘givens’ contained in the statement, but also addresses gaps we feel were left unfilled. In the end, our goal is to provide the reader with a more clinically complete focused framework for concussion management.

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FILLING IN THE GAPS

There are several issues we feel are not specifically addressed by the 3rd International Consensus Statement on Concussion in Sport, yet which are essential to our understanding of concussion. Perhaps filling in these gaps will help clinicians provide athletes with the best possible concussion care.

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Brains Are Individual and Dynamic

Consider the following hypothetical experiment. One hundred athletes, matched by gender, age, muscle strength, and conditioning, are given the exact same blow to the head with the force of a typical contact sport collision. Would we predict the same outcome in all 100 athletes? Common sense and experience tell us no. Some would be concussed and some would not. Of the concussed, we would expect presentations to vary in type, severity, and duration of signs and symptoms. Although this point may seem obvious, too often we find that the brain is discussed in theory and studied clinically as if it possesses a rather narrow range of phenotypes. Compared to other organs or body parts, however, the brain possesses a tremendous interindividual range and complexity of function. Our own experience suggests there exists a set point, a threshold, for concussion that varies between individuals. We are just beginning to identify possible relationships between the concussion threshold and an array of familial and clinical factors.7,8 Developing a greater understanding of the factors that may be related to a concussion threshold should allow us, in turn, to better understand an individual's risk.

If we accept the concept that concussion risk is individualized, what can we say about the stability of that risk? If we consider an individual athlete playing in a contact sport, do we suspect that blows to the head of similar type and severity will produce a consistent result each time? Or, is it our experience that some injuries will result in concussion and some will not, regardless of how similar they appear? Our clinical experience tells us the answer is the latter. There is good evidence to suggest that an individual's concussion risk is dynamic. Neurologists know from other disease states that brain function varies in the setting of metabolic disturbance.9 Other cortical dysfunction diagnoses, such as epilepsy and migraine headache, are thought of as “threshold” diseases that can be greatly influenced by an individual's metabolic state. Among athletes, we should be aware that concussion thresholds likely vary under the influence of a variety of factors such as sleep deprivation, dehydration, and fatigue. Comorbid states (infection, depression, diabetes, among others) might also play significant roles. This clinical variability, both within and between athletes, places an added burden on the skills of the physicians and athletic trainers, suggesting a need for introspective, experimental, and evidenced-based thought, as well as excellent objective skills to be applied over all phases of care. The management of concussions in sport does not lend itself to ‘cookbook’, ‘cubbyhole’, or over-simplistic approaches to diagnosis or treatment, much less management of the same.

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Concussion is Not a One-Time Event

The Consensus Statement takes great care to define concussion as “…a complex pathophysiologic process affecting the brain, induced by traumatic biomechanical forces.” We would argue that a concussion is an ongoing process initiated by a physical force applied to the brain and that this process can last from hours to weeks. This is in contrast to the popular view that concussion is an injury that occurs at the time of impact and that symptom resolution and recovery proceed down a fixed, although hard to predict, path. Although the pathophysiologic details are unknown, it is clear that while the brain is in a concussed state, it continues to be more vulnerable to repeat injury and symptom exacerbation.

Consider, again, our hypothetical 100 athletes who receive “identical” impacts. We would expect varying outcomes based not only on their intrinsic concussion thresholds, but also on the many factors that influence them. If we posit that our 100 athletes have the same intrinsic thresholds and factors at the time of impact and follow them forward, would we expect identical outcomes? Again, the answer is no. This is because these same factors continue to influence the concussion mechanism, to varying degrees, throughout the natural history of the injury.

When a piece of brain is robbed of blood supply, the result is dead tissue, an ischemic stroke. For the first few days after the initial event, there exists an area of tissue around the stroke that remains at risk of dying, the ischemic penumbra. This area of tissue is susceptible to a variety of physiologic factors such as perfusion pressures, body temperature, and blood glucose levels. The duration of this susceptibility lasts until the brain has adjusted hemodynamically.

In concussion, there is no area of cell death, or even an established type of physical injury. The injury is physiologic. Like a stroke, however, each individual concussion produces an initial injury that, if taken in isolation, would produce a fixed set of symptoms for a fixed amount of time. Also like a stroke, there exists a period of susceptibility that follows the initial event during which a variety of factors can alter the clinical outcome. In a way, this concept can be thought of as a concussive penumbra. While the concussive mechanism is ongoing, the practical application of this concept may be to limit, to the extent possible, any physiologic stressors, such as physical exertion, mental exertion, sleep deprivation, dehydration, and hypoglycemia.

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Role of Exercise as a Stressor in Concussion Recovery

One of the more obvious and commonplace factors that can affect the natural history of concussion in the athlete is physical exertion. It is easy to imagine how increases in heart rate, oxygen demand, and glucose demand place more physiologic stress on the injured brain as it responds to exercise. An injured brain may not be able to produce an appropriate physiologic response to an exercise stimulus.

Guskiewicz demonstrated that 33% of athletes diagnosed with concussion who returned to play in the same contest in which they were injured experienced a delayed onset of symptoms at 3 hours postinjury. Only 12.6% of those who did not return to play experienced this delayed pattern of symptom presentation.10 Could exercise, as a stressor, delay return to normal neuropsychological function? This is an important consideration: Minimizing recovery time remains a sought-after goal in sport and academic studies. Furthermore, if exercise is a stressor in the concussed brain, could said exercise be mental as well as physical? Cognitive impairment appears to be prolonged in injured student athletes involved in the “mental exercise” of active learning. Perhaps we need to rethink our management of concussion as a result. Should we minimize central nervous system input in the acute recovery stage of concussion to maximize recovery?

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The Brain Awareness Problem

Clinicians frequently encounter the athlete, especially in contact sports, who works to conceal or minimize concussive symptoms in order to stay in the game. Concussion remains a diagnosis that is dominated by the subjective information supplied by an injured athlete, while the clinician seeks objective data to support their clinical decisions. It is well accepted, therefore, that concussion management is significantly affected by the “honesty” of the patient. In the acute setting, there is another mechanism at play that also can contribute to clouding of the patient's history but is rarely discussed in the concussion literature. It is a version of the concept of anosognosia, the state of being unaware of one's own neurologic deficit. In more practical terms, it is a loss of introspection by an injured brain. This phenomenon has been described in a wide variety of diseases and injuries in the brain and is thought to be caused by damage to very particular brain structures. Being unaware of any difficulties, the injured athlete may deny any and all symptoms, even in the setting of an acute concussion with obvious objective findings, yet they are, in no way, being “dishonest” while doing so.

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Neuropsychological Testing: an Imperfect Tool

Section 3 of the Consensus Statement highlights several investigative modalities, including neuropsychological testing, that should be part of the sports clinician's toolkit. Although we agree that the appropriate application of neuropsychological (NP) testing in concussion can be of clinical value, such testing does not occur in a vacuum. As a direct result of the complexity, individual variability, and plasticity of brain function, there are variables, both internal and external, that can affect NP testing results, creating significant ambiguity when using those results in clinical decision making.11 Some now feel that better-conditioned athletes achieve better baseline NP scores. Echemendia (personal communication, 2008) suggests that, within a sport, different skills required for different positions lead to different problem-solving abilities. Even different sport cultures appear to provide different baseline NP scores-athletes from the Big 10 versus the Ivy League (faster reaction time vs greater executive function) (R. Echemendia, personal communication, 2008). What degree of certainty does the clinician have that the NP data before them are true measures of brain function? If we assume that certainty to be high, can that data be adequately compared to previous testing to measure true change or a lack thereof? The value of NP testing lies in the potential objective data that it can provide. We suggest that an awareness of the factors that can affect NP results is essential to the appropriate clinical use of this important modality. Key to the quality of any NP data is controlling the environment of the subject. External distractions such as music, conversations, or television take away from the brain's ability to focus on an appointed task. Realizing the limitations of available time and resources, NP testing should be performed at individual work stations as much as possible and not in a group or classroom environment. Equally important is controlling for any “internal” variables that may affect brain function. An individual's ability to stay mentally focused is altered in situations of sleep deprivation, fatigue, or medication use, but may also be dependent on numerous physiologic variables such as body temperature, fluid status, and electrolyte levels. Whether one is performing a preseason baseline test or a postconcussion follow-up study, having an awareness of the wide variety of factors that can affect NP tests is critical to maximizing the quality of the data. Collecting good data is only the first step. The clinical relevance of that data depends on the ability to accurately measure change. Care should be taken to ensure that the tests are performed under similar conditions each time controlling, where possible, for variables, both internal and external. Only then can the clinician begin to feel confident that the results of NP testing have real clinical value. If NP testing does result in data that demonstrate significant change and that data is felt to be of adequate quality, the next pitfall lies in concluding that the change is the result of the concussion itself and not of another comorbid condition. Similarly, if NP testing shows no change from the concussion baseline, one must also consider the possibility that the result is a false negative. It is relatively common to see improvement of NP scores in the postconcussion setting, most likely as the result of increased motivation to do well. This effect could be “covering up” an otherwise identifiable change from baseline. It is worth noting that all of these issues are well known in the field of NP testing.

NP testing should be performed in a controlled clinical setting. We have at our disposal a potentially powerful source of objective data and should do everything in our power to make it as credible a test as possible.

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CONCLUSION

We know more about concussions than ever before. We are aware of the ramifications of mismanaging concussions, and concussions are no longer trivialized. All in sport understand the seriousness of this injury. But many questions remain: What of the long-term effects of concussions, the cumulative effects of multiple injury, varying treatment possibilities, or the relative predictive value of certain postconcussive signs and symptoms? The need for clarification of these issues remains.

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UNIVERSAL GUIDELINES

The theme of this editorial comment should be clear: All concussions need to be handled individually. That being said, using the framework put forth by the 3rd International Consensus Statement on Concussion in Sport permits us to offer some particular “universal guidelines” that can guide the management of every athlete with a concussive injury:

1. Every concussed athlete must be removed from competition.

2. No concussed athlete shall return to play until asymptomatic.

3. Following any concussive injury, immediate, repeated assessment and close follow-up is necessary.

4. Any concussed athlete whose condition deteriorates should be moved rapidly to a hospital for further evaluation and investigation.

5. Any athlete suffering “prolonged LOC” (loss of consciousness) or seizures shall be disqualified from the contest.

6. Every unconscious athlete should be treated as if having an unstable neck injury.

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REFERENCES

1. McCrory P, Meeuwisse W, Johnston K, et al. Consensus statement on concussion in sport, the 3rd international conference on concussion in sport, held in Zurich, November 2008. Clin J Sport Med. 2009;19:185-200.

2. Aubry M, Cantu R, Dvorak J, et al. Summary and agreement statement of the 1st international symposium on concussion in sport, Vienna 2001. Clin J Sport Med. 2002;12:6-11.

3. McCrory P, Johnston K, Meeuwisse W, et al. Summary and agreement statement of the 2nd international conference on concussion in sport, Prague 2004. Clin J Sport Med. 2005;15:48-55.

4. NIH Consensus Methodology. Available at: http://consensus.nih.gov/ABOUTCDP.htm. Accessed July 6, 2009.

5. Shaneyfelt T, Centor R. Reassessment of clinical practice guidelines: Go gently into that good night. JAMA. 2009;301:868-869.

6. Sniderman A, Furberg C. Why guideline-making requires reform. JAMA. 2009;301:429-431.

7. Gordon KE, Dooley JM, Wood EP. Is migraine a risk factor for the development of concussion? Br J Sports Med. 2006;40:184-185.

8. Schulz MR, Marshall SW, Mueller FO, et al. Incidence and risk factors for concussion in high school athletes, North Carolina, 1996-1999. Am J Epidemiol. 2004;160:937-944.

9. Posner J, Saper C, Schiff N, et al. Diagnosis of Stupor and Coma. 4th ed. New York: Oxford University Press, 2007.

10. Guskiewicz K, McCrea M, Marshall S, et al. Cumulative effects of recurrent concussion in collegiate football players: The NCAA Concussion Study. JAMA. 2003;290:2549-2555.

11. Broglio S, Macciocchi S, Ferrara M. Neurocognitive performance of concussed athletes when symptom free. J Athl Train. 2007;42:504-508.

© 2009 Lippincott Williams & Wilkins, Inc.

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