By Jack Barrow, Vijay Agarwal, M.D., and Daniel L. Barrow, M.D.
Over the past two decades, there has been increased awareness, interest, and scrutiny of traumatic brain injury (TBI), especially sports related concussion (SRC).1-4 Much of this recent interest has been fueled by reports in the lay press of the potential effects of repetitive head injury in high-profile athletes, particularly in the National Football League (NFL). TBI is defined as a penetrating injury or a blow to the head that disrupts normal brain function. TBI is the leading cause of death and disability in war zones.5 In the civilian population, causes include falls, transportation accidents, construction accidents, sports, and domestic violence.6,7Â The description of chronic traumatic encephalopathy (CTE), a neurodegenerative disease thought to be caused, at least in part, by repetitive brain trauma, has further increased public awareness and raised fear about the potential cumulative effects of concussion in children and adolescents.8 Because of the increased public awareness of the long-term health implications and need for medical evaluation and treatment, all physicians should be aware of the current state of the field.
This article focuses on concussion, also known as mild TBI, and does not specifically address severe cases of TBI that may result in extended periods of unconsciousness, coma or even death. The Centers for Disease Control and the World Health Organization have recommended the term “concussion†be replaced by “mild traumatic brain injury.†Although these terms have been used interchangeably, the term concussion is more commonly used in athletic circles.9 Concussion is the most common type of TBI, accounting for as much as 75% of all cases.1 Although younger individuals are more likely to be the victims of TBI, there has been a recent shift in the incidence of TBI toward older individuals, with falls being the primary cause in this population.10,11 Males are significantly more prone to experience TBI than females in every age group.2,3,12 It is estimated there are up to 3.8 million instances of SRC in the U.S. in any given year.5,13,14 The increase in sports and recreation-related concussions is partly due to increased awareness of the condition, with annual estimates increasing from 300,000 in 2001 to nearly 4 million in 2011.15,16 Even with increased awareness, concussion is often underdiagnosed and easily overlooked.9,11 Since many people are not evaluated in a medical setting, the true annual incidence of mild TBI is thought to be much higher. The problem is compounded by the fact that: concussions may be asymptomatic in its most benign form, there are typically no structural abnormalities on conventional imaging studies, and many of the most common symptoms are subjective with an unknown number of athletes minimizing their complaints to avoid removal from play.9,17,18
Pathophysiology and Consequences
Despite its prevalence, our knowledge of many of the basic features of concussion is incomplete and there is lack of agreement on many issues involving concussion. There is not even consensus on the definition of concussion. In 1993, the American Congress of Rehabilitation Medicine (ACRM) defined concussion as having “any alteration of mental state at the time of the accident (dazed, disoriented, or confused).†This diverged from earlier definitions because it did not require a finding of loss of consciousness to establish the diagnosis of TBI. Instead, it identified four alternative acute events to meet the definition: LOC, change in mental state, amnesia, or focal neurological deficits. See Table 1.
The biomechanics of concussion are also poorly understood and disputed among experts. Sudden acceleration or deceleration of the brain within the cranium or a complex combination of both movement and sudden impact results in the primary injury to the
brain. The primary injury is believed to be neuronal damage at the time of the impact. The brain dysfunction and resultant symptoms of concussion, however, appear to be the result of rotational forces exerted at the junction of the upper midbrain and thalamus that cause transient disruption of the neurons that maintain alertness.19 Also, the cause of the amnesia that may be associated with concussion is not known. In addition to the damage caused at the moment of injury, a variety of events in the minutes to days following the injury may result in secondary injury, which may result in neuronal damage caused by subsequent physiological processes. This includes alterations in cerebral blood flow and pressure within the skull.
Historically, the severity of TBI has been most frequently evaluated with the Glasgow Coma Scale (GCS).12 Mild TBI is defined as a GCS score of 13–15, moderate TBI is defined as a GCS score of 9–12, and severe TBI is defined as a GCS score of 8 or less. See Table 2.
Symptoms of Concussion
Symptoms of a concussion are often nonspecific and include headache, confusion, imbalance, dizziness, sleep disturbance, or difficulty with school or work. Often the symptoms are vague and patients may describe such things as being “in a fogâ€. Some may demonstrate amnesia after a concussion, the extent of which roughly correlates with the duration of loss of consciousness. The amnesia may be both anterograde (inability to retain new information) and retrograde (difficulty in recalling memories). Retrograde amnesia is typically for the moments before injury, but in unusual cases it may extend for longer periods. In some cases, concussion does not cause a loss of autobiographical information, such as one’s name and birth date.19 When it is seen, this type of memory deficit is a symptom of hysteria or malingering. A single brief convulsion may occur immediately after a concussion. Football players have been witnessed to exhibit what has been termed “fencing posture†shortly after a concussive blow. The mechanism is not known, but a brief convulsion or fencing posture neither portends epilepsy nor requires anticonvulsant medication.19
Postconcussion syndrome
A significant proportion of concussed patients will report persistent symptoms after concussion, including headache, cognitive dysfunction, dizziness, fatigue, and irritability. This cluster of rather non-specific symptoms has been termed the postconcussion syndrome (PCS), a condition long recognized but still controversial.20 The incidence, frequency, pathophysiology and natural history of this disorder is unclear. In some instances, symptoms may persist for months and can be challenging to treat, although the symptoms typically resolve gradually over time. It is as yet unclear whether post-concussion syndrome is the result of structural abnormalities or organic cerebral dysfunction.21,22 In an investigation in which an MRI of the brain was performed within 24 hours and after 3 months in 20 patients who had suffered a concussion with a verified loss of consciousness, patients were compared to a control group of 20 participants with minor orthopedic injuries patients who were matched for age and gender and underwent MRI investigation using the same protocol.20 No significant intracranial traumatic pathology was detected in any of the concussed patients. The authors concluded that a concussion with a short-lasting loss of consciousness does not, or seldom, results in diffuse axonal injury visualized by conventional MR imaging. Whether advanced imaging with higher field strength or more sensitive imaging would identify structural abnormalities remains to be determined.
Good data from randomized controlled trials does not exist to assist in the management of PCS. Instead, patient and family education, reassurance, and symptomatic management is the common course of therapy.23 Headaches should be managed with non-narcotic analgesics and dizziness should be managed with vestibular exercises. These patients are not uncommonly placed on antidepressants for symptom relief, but there is little data to support their use.
The Role of the Physician
In October 2006, Zachary Lystedt, a 13-year-old middle school football player suffered a concussion, collapsed, and was allowed back into a game. Walking away from the field after the game with his father, Zack collapsed and was airlifted to Seattle’s Harborview Medical Center, where he underwent a decompressive craniectomy and evacuation of bilateral hemorrhages. On May 14, 2009, Governor Christine Gregoire signed the Zackery Lystedt Law for the state of Washington. It is the most comprehensive return-to-play law in the United States for athletes under the age of 18 years and, although not all as rigorous, all 50 states and the District of Columbia have passed similar laws. The main tenets of these laws include: informing and educating young athletes and their parents, and requiring them to sign a concussion information form; removing of a youth athlete who appears to have suffered a concussion from play or practice at the time of the suspected concussion; and requiring a youth athlete to be cleared by a licensed health care professional trained in evaluation and management of concussions before returning to play or practice. With the increased attention to SRC, physicians of all types are playing a larger role and many come in contact with concussed patients at various stages of injury. Pediatricians, general practitioners, and internists are asked to provide medical screening for various athletic activities. Neurosurgeons, emergency room physicians, neurologists, orthopedists, and physiatrists are requested to be present on the sidelines to evaluate athletes with SRC and to determine if it is safe to resume play. Physician-scientists and academic physicians are performing the clinical and basic research necessary to advance our understanding of the mechanisms, pathophysiology, clinical manifestations, treatment and sequelae of TBI.
Medical Clearance of Athletes with Concussions
When evaluating an athlete with a history of concussion, the physician should attempt to determine the total number of concussions they have experienced, the duration of symptoms, the frequency and time interval between concussions, and recovery time. Neuroimaging is generally not recommended, but a complete neurologic examination should be performed and, if the patient has any focal neurological deficits, imaging may be indicated. Athletes with signs and symptoms of concussion or postconcussion syndrome should not be cleared for participation until all symptoms have resolved.24 Formal balance testing, such as the Balance Error Scoring System and neuropsychologic testing, can help inform decisions about when to return to play. However, there are no universally agreed upon criteria for disqualifying athletes with a history of frequent or severe concussions and decisions must be individualized.25
Sideline Evaluation
In some scenarios, physicians will be asked to be physically present during contact sports to evaluate patients suspected of suffering a concussion and to assist in the decision to return to play. One of the most noteworthy examples is the Unaffiliated Neurotrauma Consultant (UNC) program instituted by the National Football League (NFL) in conjunction with the NFL Players Association (NFLPA) in 2013. The UNC Program and the Independent Athletic Trainer Spotter (ATC) Program were developed to improve sideline medical care on game day. UNCs, who are independent of either club, are involved in all in-game neurological assessments. Beginning in the 2018 season, all NFL are required to have a UNC on each sideline and a third in the press box. Additionally, independent ATC spotters in the press box are empowered to call a medical timeout to stop the game and have a player receive medical attention should they show signs of distress or disorientation. When evaluating a patient at the scene of the injury, the airway should be kept clear, and if the mechanism of injury suggests spine trauma or patient has any neck pain, cervical immobilization is required. There are certain symptoms and signs that are clear and unequivocal signs of disqualification from further play, or what is referred to as a “No Goâ€. This includes loss of consciousness or unresponsiveness, confusion, anterograde amnesia, new and/or persistent symptoms, seizure activity or fencing posture, diplopia, repeated vomiting, or focal neurological deficits.
Although there are numerous objective assessments for concussion, no single test has been validated as the gold-standard diagnostic.26 One internationally accepted method of measuring the severity of concussion is the Standardized Assessment of Concussion (SAC) developed in 1997. This was developed to address the need for an objective and standardized assessment of concussion, and includes screening of neurocognitive and neurological functions in addition to symptom assessment.27,28 At the Second International Conference on Concussion in Sport in 2004, the SAC was combined with a standardized symptom scale, sport-specific orientation questions and an expanded list of indicators of concussion. Along with guidelines for a systematic, stepwise return to play this became the first iteration of the Sport Concussion Assessment Tool (SCAT).29 In the most recent revision (SCAT3), published in 2013, additional physical/objective signs (i.e., blank/vacant look, cervical stability assessment) were added with the option of using either foam stances or a timed tandem gait task for postural stability assessment.30 In addition, a SCAT3 version tailored to children (age < 13 years) was introduced, the Child-SCAT3.31
The duration and setting of monitoring the concussed patient must be individualized and based upon the mechanism of injury, neurological examination, and period of unconsciousness and amnesia. Patients with a normal neurologic examination are generally observed for approximately 2 hours and safely discharged to the care of a responsible person.32-34 Those suffering from concussion should return for further medical care and evaluation 24 to 72 hours after the event, and sooner if the symptoms worsen. Athletes, especially at the collegiate or professional level, are usually followed closely by team physicians or athletic trainers during this period, but others may need to follow up with their primary physician. It is helpful to provide instructions with symptoms that should be monitored for a prompt return to the hospital, such as increasing headache, repeated vomiting, weakness, clumsiness, drowsiness, or fluid from the nose or ear that might represent a leak of cerebrospinal fluid. Headache and mild cognitive difficulty are common for a day or more after concussion. Whether it is necessary to awaken a patient at night to confirm that he or she can be aroused has not been established. It is generally recommended that patients not resume normal activity until they are free of headache and other symptoms such as dizziness. Increasingly, to assist in the decision to return to play, athletes are undergoing pre-season testing to provide a baseline for comparison in the event of an injury.35 If baseline testing is available, return to play decisions are more objective and return is withheld until the athlete returns to their baseline test results.
Criteria for Cranial Imaging
Less than 10% of patients experience a brain bleed after a concussion, and less than 2% require neurosurgical intervention.36 Non-contrasted cranial computed tomography (CT) is adequate to detect significant intracranial bleeding; magnetic resonance imaging is not necessary for this purpose. Clinical decision (or prediction) rules are derived from original research and is defined as a decision-making tool that incorporates 3 or more variables from the history, physical examination or simple tests to assess status. The overall goal is to reduce the uncertainty of medical decision-making by standardizing the collection and interpretation of clinical data.37 The New Orleans Criteria (NOC) and the Canadian CT Head Rule (CCHR) are two such decision rules that have been independently developed to allow more selective ordering of CT scans, more rapid discharge of patients with minor head injury, and significant health care savings.32,38 See Table 3.
In two large prospective studies of minor head injury, the presence of any of the clinical features in these rules identified essentially all patients requiring immediate neurosurgical intervention.32,37 A lower threshold should be maintained for young children, intoxicated patients where clinical manifestations may be obscured, for anticoagulated patients, and for those who cannot be reliably observed after evaluation. In those patients meeting criteria for CT imaging, certain findings influence care and management. A fracture across the groove of the middle meningeal artery is associated with a higher risk for epidural hematoma. Small contusions or small traumatic subarachnoid hemorrhages occur in approximately 5% of patients, and are usually managed conservatively without sequelae other than headache, but do require more prolonged observation and perhaps follow up imaging.
Management of Concussion Symptoms
Treatment generally involves physical and cognitive rest until symptoms resolve with a gradual return to activities. Cognitive rest includes reducing activities such as school work, video games, and text messaging which require concentration and attention.31 Prolonged periods of rest may actually worsen outcomes.39 Physical therapy may be useful for persistent balance problems while cognitive behavioral therapy may be useful for disorders of mood. It is important to stress the importance of avoiding another head injury during the recovery period as another concussion before the symptoms of a prior concussion have resolved is associated with worse outcomes. For persons participating in athletics, the 2008 Zurich Consensus Statement on Concussion in Sport recommends that participants be symptom-free before restarting and then progress through a series of graded steps, including:
• complete physical and cognitive rest
• light aerobic activity (less than 70% of maximum
heart rate)
• sport-specific activities such as running drills and
skating drills
• non-contact training drills (exercise, coordination, and cognitive load)
• full-contact practice
• full-contact games
Only when symptom-free for 24 hours should progression to the next step occur. If symptoms occur, the person should drop back to the previous asymptomatic level for at least another 24 hours. The emphasis is on remaining symptom-free and taking it in medium steps, not on the steps themselves.31
Research and Future Advances
Neurosurgeons have been pivotal in the recognition, management, implementation, of rules changes, research in sports concussions. Academic programs use TBI labs clinics to explore effects of repeated TBI, improve detection methods and diagnostic tools. The clinical exam (GCS) and CT scans are useful, but antiquated. Need blood-based biomarkers and MRI bio-markers to diagnose TBI. Need a better TBI classification. “Mild, moderate and severe,†based on GCS is antiquated, inadequate. Need a better understanding of long-term sequelae of TBI. TBI is a process, not an event. “Mild†TBI outcomes (GCS13-15) are not mild for those with pathology on CT and/or MRI scans. Relationship between TBI and Parkinson’s, Alzheimer’s, CTE, PTSD, and depression needs exploration. Studies even implicate TBI in brain tumor development.40,41 Authors proposed TBI incites an inflammatory response linked to oncogenic transformation of progenitor and neural stem cells that migrate to the injury site. Although controversial no definitive pathogenesis proposed.
Conclusions
There has been significant interest in the awareness, diagnosis and treatment of TBI over the past 20 years. Due to these advances, athletes, particularly those in youth sports, have received more effective treatment for their head injuries. What is clear, though, is that the more we learn, the more we realize just how much more work needs to be done to completely understand the pathophysiology of TBI and optimally treat those who experience these symptoms.
Note: The senior author (DLB) is an Unaffiliated Neurotrauma Consultant for the National Football League
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