Any sport has an inherent risk of injury. A balance must be reached between maintaining a competitive edge in a sport and ensuring participant safety. Frequently the loss of objectivity on the part of the athlete, coaches, sports media, and spectators is an unfortunate and potentially harmful bias. In that setting, the health professional's role is to provide objective assessment of the injured athlete and guidance about the advisability of safe return to competition.
There are three main issues that should be addressed by any guideline for the management of concussion. The health outcomes that need to be addressed at the time of the injury and during the follow-up period include (1) the appropriate management of the injured athlete at the time of injury to identify potential neurosurgical emergencies (epidural, subdural, and intracerebral hemorrhages); (2) the prevention of catastrophic outcome related to acute brain swelling; and (3) the avoidance of cumulative brain injury related to repeated concussions.
Mild traumatic brain injury typically does not require neurosurgical intervention, and the treatment of postconcussion symptoms often falls to the neurologist. [1] Questions addressed during neurologic or neurosurgical consultation for sports-related concussion call for advice to the patient that is guided by neuroscience and the consensus of experts, rather than local lore and individual opinion. Most importantly, consultation regarding the prevention of catastrophic outcome and cumulative neurobehavioral deficits from repeated concussions can best be provided by the well-informed physician. This report, based on a project already completed by the Colorado Medical Society, [2] was written to provide background information for a practice parameter of the American Academy of Neurology (AAN). [3]
Disagreement about the terminology of mild traumatic brain injury and concerns about the proper management of sports-related concussion led to the development of this document. Several articles and textbook chapters have appeared in the literature in recent decades dealing with the issue of sports-related concussion. These usually have been written by sports-medicine specialists or neurosurgeons who serve as athletic team physicians or consultants. Their approach to sports concussion has been pragmatic and sensible, based primarily on their own experiences. Unfortunately, their experiences tend to be anecdotal and isolated from one another, with little attention paid to animal-experimentation literature or our evolving understanding of the pathophysiology of traumatic brain injury. In addition, there had been no formal process for building consensus among experts prior to the development of the AAN practice parameter, which offers a grading scale for concussion based on severity of injury. [3] This parameter has been widely endorsed by medical specialists and national organizations. The adoption of a single concussion grading scale is essential to the advancement of clinical research into the incidence of concussion, patterns of recovery, risks of neurosurgical emergencies, and the development of permanent neurologic dysfunction.
Concussion is a common consequence of trauma to the head in contact sports, but it can result from collisions or falls in all forms of athletic activity. It can also occur without a direct blow to the head if sufficient force is applied to the brain in a "whiplash" mechanism injury. [4] President Theodore Roosevelt's fury over the 19 athletes who were killed or rendered paralyzed in 1904 from football injuries led to the formation of the National Collegiate Athletic Association [5] as a governing body to establish rules for safer athletic competition. Even so, fatalities at all levels of football peaked at 30 in 1964, [6] the majority from head and neck injuries. More recent rule changes, protective-equipment improvements, and coaching techniques emphasizing injury prevention have been helpful in reducing the incidence of traumatic brain injury. [5]
The rates of concussion in some popular collegiate sports are listed in Table 1 and Table 2. [7] Earlier estimates of concussion in the game of football played at all levels put the number at 250,000 per year in the United States alone. [8] This number was based on a survey that found 20% of high school football players had sustained some form of concussion. [9] Ten percent of the college football players sustained concussion in one other study. [10] Current estimates of the incidence of concussion in football at all levels suggest that about 100,000 per year may be more accurate. [11] No matter whose estimates are used, the dimension of this problem warrants more attention than it has received thus far.
Table 1. Sports with helmets
Table 2. Sports without helmets
The National Football Head and Neck Injury Registry [12] documented a yearly average of eight deaths caused by head injuries between 1971 and 1984 at all levels of football. Some players suffer two or more concussions. The risk of sustaining a concussion in football is four [9] to six [13] times greater for the player who has a history of concussion than for the player who has no history of concussion. Repeated concussions have been shown to impart cumulative neuropsychological [14] and neuroanatomical [15,16] damage, even when incidents are separated in time by months or years.
Consensus process.
Literature reviews and analyses of the available evidence were discussed on numerous occasions by the Quality Standards Subcommittee (QSS) of the AAN and sports-related concussion symposia faculty, and at meetings with physicians from specialties representing sports medicine, emergency medicine, orthopedics, neurosurgery, neurology, physiatry, pediatrics, and neuropsychology, as well as representatives from allied health fields, including athletic trainers and paramedics. The evidence for and against the outcomes was balanced and a recommendation put forth. Initially, the draft was reviewed and revised by the various organizations consulted by the members of the AAN-QSS. A grading scale was created based on scientific evidence and consensus.
In 1996, two meetings were held to obtain critical review and feedback regarding this document in its final stages of development. The first meeting was held on March 22, 1996, in Pittsburgh, during the seminar entitled "Sports-Related Concussion: Neurological and Neuropsychological Evaluation and Management," hosted by the Allegheny General Hospital. The participants in this conference are experts involved in the treatment of athletes who have sustained concussion. The second meeting was of a similar group of individuals who met at the annual meeting of the American Association of Neurological Surgeons on April 28, 1996, in Minneapolis. Discussions at these two meetings led to further clarifications regarding the identification and grading of concussion and criteria for return to play. A list of participants in these meetings is provided in the publication, "Practice Parameter: The management of concussion in sports." [3]
The AAN has called for the ban of boxing, a position taken by many physician organizations in this country and abroad. These recommendations for the management of concussion in sports are not intended to justify boxing as a legitimate sport, nor should they be construed as in conflict with the official stance of the AAN. [17]
Evidence.
A Medline search from 1966 through 1996 was carried out with the following key terms: "athletic injuries" and "brain concussion." This resulted in 10,980 articles cited on Medline, which were narrowed to 71 articles by the intersection of the two key terms. The abstracts of all 71 citations were reviewed. The articles were retrieved that specifically dealt with concussion and sports. The available evidence was divided into class I, II, and III evidence with use of the following definitions:
Class I: Evidence provided by one or more well-designed randomized controlled clinical trials.
Class II: Evidence provided by one or more well-designed clinical studies.
Class III: Evidence provided by expert opinion, non-randomized historical controls, case series, or case reports.
Based on the strength of this information, management recommendations [3] have been made as practice options using the following definitions:
Standards: Generally accepted principles for patient management that reflect a high degree of certainty that is based on class I evidence; or, when circumstances preclude randomized clinical trials, overwhelming evidence of class II studies that directly address the question.
Guidelines: Recommendations for patient management that may identify a particular strategy or range of management strategies and that reflect moderate clinical certainty based on class II evidence or strong consensus of class III evidence.
Options: Other strategies for patient management for which there is unclear clinical certainty (i.e., based on inconclusive or conflicting evidence or opinion).
Definition of concussion.
Concussion is a trauma-induced alteration in mental status that may or may not involve loss of consciousness. [18] The misunderstanding that concussion requires loss of consciousness has surfaced again in recent years. More than 30 years ago, the Congress of Neurological Surgeons [19] concluded that head injury leading to mental status alterations without loss of consciousness is also a form of concussion. C. Miller Fisher [20] also offered a clear case of amnesia from head injury without loss of consciousness, and he alluded to numerous other reports in his experience and in the literature of similar cases. Ommaya and Gennarelli [21] created an animal model of traumatic brain injury in which three of the six grades of concussion did not involve loss of consciousness. More recent animal studies [22] also found axonal swelling after mild traumatic brain injury in animals, further demonstrating that neuroanatomic alterations indeed occur during concussion.
Confusion and amnesia are the hallmarks of concussion. Although disorientation may be present during a confusional state, more subtle abnormalities are typical. The cardinal features of confusion include (1) disturbance of vigilance with heightened distractibility, (2) inability to maintain a coherent stream of thought, and (3) inability to carry out a sequence of goal-directed movements. [23] The confusional episode and memory dysfunction may be immediate following the blow to the head [20] or may be a delayed process taking several minutes to fully evolve. [24] Close observation and assessment of the athlete over some period of time is necessary to see if the evolving neuropathologic change associated with concussion leads to physical signs and symptoms or to the development of memory dysfunction. Neurobehavioral features observed in concussion are listed in Table 3, and symptoms typically reported are listed in Table 4. The history of recent head trauma outside the sports setting, such as a motor vehicle accident, should be considered in the evaluation of any athlete with concussion.
Table 3. Frequently observed features of concussion
Table 4. Symptoms of concussion*
Acute injury management.
Managing the concussion victim is essentially no different from any other emergency procedure. A process of evaluating the athlete for serious signs and symptoms must occur in an orderly and systematic fashion. Any worrisome signs or symptoms must be identified quickly, and evidence of intracranial pathology must be recognized and dealt with emergently. Prolonged unconsciousness, persistent mental status alterations, worsening post-concussion symptoms, or abnormalities on neurologic examination require urgent neurosurgical consultation or transfer to a trauma center. Neuroimaging of the athlete with any of these concerns should be performed emergently. These are general rules of neurosurgical care of patients who have sustained traumatic brain injury, not specific to any problems athletes may suffer. [25,26] All athletes suspected of having sustained concussions should undergo thorough evaluation, including mental status testing, neurologic screening examination, and exertional provocative maneuvers as outlined in Table 5.
Table 5. Sideline evaluation
Second impact syndrome.
The "second impact syndrome" [27] is thought to be the result of a second concussion occurring while the individual is still symptomatic from an earlier concussion. [18,28-30] In second impact syndrome, the athlete suffers cerebrovascular congestion, or a loss of cerebrovascular auto-regulation, leading to malignant brain swelling and marked increase in intracranial pressure. Animal research has shown that brain swelling from vascular engorgement after head injury is very difficult, if not impossible, to control. [31,32] Although brain swelling is more commonly seen in the pediatric age group, [33] it also occurs in young adults. [18,28]
It is widely accepted that any symptoms of post-concussion effect preclude the athlete from returning to contact sports. [34] Prematurely returning to contact sports, or any sport in which head injury is a risk, could lead to a catastrophic outcome such as permanent disability or death (Table 6). Decisions to return to play must also be addressed in an orderly and systematic fashion. Health care professionals should look in detail for mental status and neurologic abnormalities that may be associated with subtle neuropathology caused by concussion.
Table 6. Evidence table for second impact syndrome (all are class III evidence)
The neuroimaging studies most likely to pick up neuroanatomic changes are MRI and CT of the brain. MRI is more sensitive to traumatic injuries of the brain. [35-37] CT is useful for documenting bleeding, swelling, [18,38] or major shifts in the intracranial compartment requiring neurosurgical intervention. When the fully evolved neuropathologic change of the second impact syndrome is detected by CT, cortical areas appear to be diffusely dense due to increased vascular volume in the brain. This has been called cerebrovascular congestion, which is indistinguishable on CT from the images of severe traumatic brain injury in children. [18,33]
Cumulative neuropsychological impairment.
For more than two decades, we have known that repeated concussions can impart cumulative neuropsychological deficits [39], i.e., increasing severity and duration of mental status abnormalities subsequent to each separate incident. These neuropsychological deficits may be evident even when no abnormalities are detectable on detailed neurologic examination. [40]
More recent evidence that repeated concussions in athletes can lead to lingering symptoms [41] and neuropsychological deficits [42] has appeared in the nonpeer-reviewed literature. These concerns have led to a heightened awareness in the athletic and medical communities that criteria are needed for the retirement of athletes from high-risk contact sports.
Conclusions.
The usefulness of a grading scale has been well established in sports medicine to determine the severity of a concussion. A review of previous sports concussion guidelines [43-46] leads to the conclusion that the subtle cognitive and behavioral changes that should be detectable by closer monitoring of the athlete were being overlooked. Frequently noted signs and symptoms of concussion are listed in Table 3 and Table 4.
Exertional tests must also be performed so that the examiner may witness the effects of a Valsalva manuever under controlled conditions prior to return to play. A screening neurologic examination is adequate on the sideline, as long as some tests of coordination, motor strength, and sensation are performed.
It is most important that an examination of mental status be performed on all athletes suspected of having sustained concussion. Mental status examination must include short-term memory tests to evaluate the athlete's ability to learn new information. Memory loss for the events following the injury (post-traumatic amnesia) or for events preceding the injury (retrograde amnesia) constitute mental status abnormalities, as would failure to retain memorized information (e.g., three words and three objects).
Because it is not the intention of this report to suggest detailed management options for the comatose patient, the reader is referred to other standard texts on this topic. [25,26] It is generally accepted that any period of unconsciousness from trauma is due to bilateral dysfunction of the cerebral hemispheres or to damage reaching the physiologic activating mechanisms within the upper brain stem and diencephalon. [47] Concussion, a mild traumatic brain injury, can no longer be the diagnosis if there is loss of consciousness for more than thirty minutes, if the initial Glasgow Coma Scale is less than 13, or if post-traumatic amnesia exceeds 24 hours. [48]
The Standardized Assessment of Concussion (SAC) [49] was developed as a brief quantifiable mental status evaluation instrument that tests attention, concentration, and short-term memory. Preseason individual baseline testing can be done to provide comparison with scores obtained later when an athlete sustains a concussion.
More detailed mental status evaluation with a battery of neuropsychological tests [42] is being used in a similar fashion by several sports organizations, allowing for even more sensitive detection of cognitive deficits associated with concussion.
In most instances when an athlete has suffered a head injury that requires intracranial surgery, return to contact sports is contraindicated. However, the final determination as to whether an athlete may return to competition is the clinical decision of the athlete's physician.
Acknowledgments
We are grateful to Carol Mester and Joanne Okagaki for their skillful assistance in the preparation of this manuscript.
- Copyright 1997 by Advanstar Communications Inc.
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