CHAPTER 332 Mild Traumatic Brain Injury in Adults and Concussion in Sports
Definition of Concussion and Mild Traumatic Brain Injury
The terms concussion, mild traumatic brain injury, and minor traumatic brain injury are often used interchangeably, and, to date, there is no universally agreed upon definition of either. One of the more commonly used definitions for mild traumatic brain injury (mTBI) arose from a meeting of the American Congress of Rehabilitation Medicine, which characterized the injury as involving an alteration in consciousness (amnesia or confusion), less than 30 minutes loss of consciousness, or less than 24 hours of posttraumatic amnesia, with focal neurological deficits that “may or may not be transient.”1 Many other definitions of mTBI involve loss of consciousness (LOC) lasting less than 20 or 30 minutes, Glasgow Coma Scale (GCS) scores of 13 through 15, and some definitions may specify that hospitalization must not be necessary or that there are no focal neurological findings. Concussion was defined as an “immediate and transient posttraumatic impairment of neural function…because of brain stem dysfunction” by the Congress of Neurological Surgeons.2 The World Health Organization Collaborating Task Force on mTBI criteria required an acute brain injury to result from mechanical injury to the head from external physical forces and at least one of the following: LOC 30 minutes or less, focal neurological signs or seizures, posttraumatic amnesia (PTA) less than 24 hours, and/or GCS of 13 to 15 after 30 minutes.3 In 1997, the American Academy of Neurology defined concussion as “any trauma induced alteration in mental status that may or may not include a loss of consciousness.”4 The Concussion in Sport Group described the injury as “a complex pathophysiological process affecting the brain induced by traumatic biomechanical forces.”5
The Centers for Disease Control and Prevention (CDC)6 recently provided a collective and comprehensive definition for concussion and mild traumatic brain injury, using the two terms interchangeably:
Efforts have been made to classify adult mild head injury to better reflect recommended evaluative courses of action.7 In this model, all acute head injured patients are referred to as having “mild head injury,” then this group is broken into three risk groups. The “low-risk mild head injury” patients have a GCS score of 15, and no signs or symptoms of loss of consciousness, amnesia, vomiting, or diffuse headache. “Medium-risk mild head injury” patients have a GCS of 15 with one or more of the earlier described symptoms. “High-risk mild head injury” patients have a GCS of 14 or 15 and have skull fracture and/or neurological deficits. Patients with risk factors of coagulopathy, history of neurosurgical procedures, history of epilepsy, drug or alcohol consumption, or age greater than 60 are included in the high-risk group regardless of the clinical presentation. These categories are based upon the risk of intracranial hematoma requiring surgical evacuation. It is recommended that medium risk MHI patients receive a CT scan, if available, and should otherwise have a skull x-ray. All high-risk patients should have a CT scan. Table 332-1 provides descriptions of various levels of TBI severity.
| Mild TBI | GCS = 3 to 8 |
| Moderate TBI | GCS = 9 to 12 |
| Severe TBI | GCS = 13 to 15 |
Epidemiology
Estimates of mild traumatic brain injury in child and adult populations vary greatly, and have ranged from 49% to 90%8,9 of traumatic brain injury in the literature. The vast majority of patients requiring hospital admission after sustaining a head injury are those with mTBI. Studies in the 1980s cited that mTBI accounts for anywhere between 49% and 82% of traumatic brain injuries treated in hospital emergency rooms.10–14 Although many mTBI patients are seen in nonhospital settings, such as physician offices, clinics, and training rooms, ultimately about 10% will require hospitalization. The long-term morbidity and mortality should be extremely low, for few of them sustain potentially serious intracranial injury. Nonetheless, the potential for major injury is omnipresent, and an organized and consistent approach serves well to ensure proper management. It has been estimated that approximately 3% of all patients having a GCS score of 13 to 15 will ultimately need a neurosurgical procedure.
Cassidy and associates8 provide comprehensive descriptions of epidemiologic studies of mild traumatic brain injury from 1980-2000. Although estimated rates vary between studies, most studies find increased rates in males and young adults, with mixed results for race. Most common causes for mTBI across studies were motor vehicle accidents, falls, or assaults. Regarding sports- and recreation-related concussions specifically, the CDC has provided recent estimates that approximately 1.6 to 3.8 million mild traumatic brain injuries occur each year,6 and that approximately 20% of all head injuries are sports-related concussions.15 Although a daunting figure, most believe this remains an underestimate of the injury, given that many concussions go unreported. By sport, American football,16 soccer, and ice hockey are often cited as having the highest concussion rates in the United States.17,18 Per 10,000 participants, rates for concussed athletes coming to emergency departments were cited as 5.22 in basketball,19 5.2 in American football,20 4.90 in ice hockey,20 and 3.1 in soccer.20 Incidence of concussion in Australian football was 3.3 per 1000 player hours. Studies of collegiate American football players have found injury rates of 0.73,21 2.818 (high school), and 3.322,23 (college) per 1000 athlete exposures during games and practices, and one study estimated that in the United States, football players alone suffer a minimum of 1.5 concussions each year.24 Studies of soccer players found a rate of 0.6 per 1000 athlete-exposures for males and 0.4 for females in a college sample,25 and game rates of 0.57 and 0.71 per 1000 athlete exposures in high school male and female games.18 Estimates of incidence in ice hockey range from 1.5 concussions per 1000 athlete game hours in a Canadian college26 sample to 17.6 per 1000 athlete game hours in a Minnesota sample of 11 to 19 year old boys.27 Concussion rates for high school boys and girls in basketball practices were listed as 0.06 and 0.07 per 1000 exposures, respectively, and were 0.28 (boys) and 0.71 (girls) per 1000 basketball game exposures.18
In most sports, the risk of concussion is most often greater in games,16,18,21 with football players being up to 14 times more likely to sustain a concussion during a game than a contact practice.21 In cheerleading, concussions happen more often in practices than in games.16 A review of epidemiologic studies of mTBI found injury rates in sports ranging from 0.62 to 8.0 per 1000 athlete game hours, and rates of 0.1 per 1000 athlete practice or game hours for those under 15 years old and 17.1 per 100 athlete practice or game hours in a sample of senior rugby players.8
In certain sports, the position played has been linked to concussion rates. In football, linebackers, wideouts, and safeties, respectively, sustained the greatest number of concussions in one study,21 with other studies rating quarterbacks,28 running backs, and defensive secondary players being more at-risk.18,22,23 In rugby, forwards had double the risk of backs for sustaining concussions.29,30
Pathophysiology of Mild Head Injury
In a review of multiple articles from scientific literature, Giza and Hovda31 described the pathophysiology of concussion, and a more detailed description of the pathophysiology of brain injury is contained in another chapter. In brief, concussion initially results in what has been described as a “metabolic mismatch,” during which cerebral blood flow significantly decreases, yet demand for glucose increases. This is the result of a process whereby excitatory transmitters bind to N-methyl-D-aspartate (NMDA), causing depolarization of the neuron during which there is an influx of calcium and an efflux of potassium. Increased excitatory activity caused by increased extracellular K+ is then followed by diffuse depression of neuronal activity. The increased adenosine triphosphate (ATP) required by the increased activity of the sodium-potassium pump working to restore the ionic imbalance leads to increased glucose metabolism.
Although glucose metabolism initially increases postinjury, a period of hypometabolism soon follows, which has been shown to persist for up to 10 days in animal studies32 and for up to 1 month in PET studies of human TBI.33 It has been postulated the hypometabolism may be linked to the lingering postconcussion the symptoms.31 In addition, mild traumatic brain injury has been linked to decreased magnesium levels, diffuse axonal injury, persistent calcium accumulation, and alterations in neurotransmitter activity.31
Research has established that, in some instances of mTBI, both cellular and ultrastructural damage may occur. Recent experiments with radioactive tracers have shown the axonal injury may occur in a nonlethal concussive model, and that progressive axonal swelling and disturbance in axonal transport results in the hours and days following the injury.34 However, the intracellular metabolic effects of mTBI have now been more firmly recognized.
Recent autopsy studies suggest chronic traumatic encephalopathy, especially tauopathy, has been seen in case studies of modern professional football players.35,36 However, further collaborative studies will be necessary.
Signs and Symptoms of Injury
Patients with mTBI may have symptoms such as headache, nausea, vomiting, or have focal neurological deficits. Seizures or clinical signs of a skull fracture are rare, but also may occur. Concussion or mTBI may go undiagnosed or may be mismanaged in part because of the variability in the type, number, and severity of injury signs and symptoms. It is important to note that, although loss of consciousness may occur with mTBI, it often is not present, and its absence would not rule out a diagnosis of concussion. At times, patients who are experiencing postconcussion symptoms have been told they did not sustain a brain injury because they did not experience a loss of consciousness. In addition to loss of consciousness, mental status changes that may be observed following mTBI include retrograde amnesia, anterograde amnesia, disorientation, confusion, or looking “dazed.” Although more rare, occasionally tonic posturing, clonic movements, and convulsions are observed following concussion.37 Symptoms of concussion can include headache, dizziness, balance problems, phonophobia, and others. See Table 332-2 for a summary of commonly reported signs and symptoms of injury. Although it is most common for symptoms to onset immediately following trauma, some patients may not experience or notice symptoms for several minutes, hours, or sometimes days after injury. A study of concussed athletes revealed a small subsample who did not experience symptom onset until about 14 to 15 minutes after injury (mean = 14.4, SD=15.5 minutes).38 Higher postconcussion symptoms acutely (72 hours) postinjury have been related to a greater likelihood of experiencing more significant mental status changes secondary to injury, including being more likely to have experienced PTA, retrograde amnesia (RGA), and disorientation or at least 3 of the following four signs: LOC, PTA, RGA, or disorientation.39
| Signs of Injury |
Further underscoring the need to attend to all symptoms was a study that explored the subtle symptom of “feeling mentally foggy” and its relation to neurocognitive performance. In this study, concussed athletes who endorsed any degree of mental fogginess had worse performance on memory, reaction time, and processing speed measures, as well as reporting an overall higher total symptom score.40
Posttraumatic Headaches
In sports-related concussion studies, headaches have been consistently cited as the most frequently endorsed symptom.39,41–44 Studies have reported postinjury headache frequencies as high as 86%,45 and headaches are more commonly reported following mTBI than more severe brain injuries.46 Posttraumatic headaches are similar to their nontraumatic counterparts and may include, but are not limited to, tension-type, migrainous, cluster-like, and mixed.47 McCrory48 was the first to identify subtypes of exercise-related headaches, which included acute posttraumatic headache.
Although the exact mechanism(s) for posttraumatic headaches remains unclear, it has been suggested that trauma may cause posttraumatic headaches by acting as a sole triggering factor, being part of the postconcussion syndrome, triggering the first event in an otherwise susceptible patient, or happening by chance.49 Migraine and mTBI are somewhat similar physiologically in that increased extracellular potassium, intracellular sodium, calcium, and chloride occur with both mTBI and migraine. Both conditions are also linked to increased release of excitatory amino acids, including glutamate.46 It has been postulated that a migraine may make one more vulnerable to a concussion.50
Endorsement of postconcussion headache has been linked to memory dysfunction, slowed reaction time, and increased overall symptoms, as well as being more likely to have experienced AGA or any mental status change lasting longer than 5 minutes.39 Furthermore, athletes who endorsed moderate-to-severe postconcussion headaches at 1 week after injury reported a significantly greater intensity of general postconcussion symptoms and showed a trend toward lower neurocognitive scores when compared with those with mild postconcussion headaches.39 An examination of cognitive test performance and symptom reporting among concussed athletes with no headaches (no HA), nonmigrainous headaches (HA), and those exhibiting posttraumatic migraine characteristics (PTM) revealed that the PTM group performed significantly poorer on all four measures of cognitive functioning (verbal and visual memory, processing speed, and reaction time) and demonstrated increased symptoms relative to the other two groups. Those with headaches, but not meeting PTM characteristics performed better than the PTM group across all measures, and worse than the no-HA group on reaction time and total symptoms.51
Loss of Consciousness
In sports-related concussion, LOC occurs rarely, and has been cited as occurring in between 8% and 19% of sports-concussion injuries.43,39 Further, prolonged LOCs (greater than 1 or 2 minutes) is much less frequent in sports-related concussion, with most LOCs being less than a minute in duration.52 Although many studies find no differences in cognitive performance when comparing those who have sustained mTBI-related brief LOC,53,54 other studies have found that patients who lost consciousness did perform more poorly on cognitive testing55 and had a greater likelihood of a longer time to return-to-play following injury.56 A study using video analysis of motor and convulsive activities following sports-related concussion found LOC to be the only risk factor for tonic posturing following injury.37
Amnesia
Amnesia may be experienced as a loss of continuous memory functioning for events immediately preceding (retrograde amnesia) or following (anterograde amnesia) a brain injury. The duration of amnesia is documented as the time between the occurrence of injury and the time at which the individual regains normal, continuous memory functioning. In assessing retrograde amnesia, the on-field staff can ask the athlete questions regarding details occurring just before the trauma. With sports concussion, questions involving, for example, the athlete’s recollection of the hit, of the play leading up to the hit, of earlier plays in the game, and of the game score before the hit are all good ways to assess retrograde memory function. It is important to determine how far backward the retrograde amnesia stretches, both in a solid (complete forgetting) and “spotty” (patchy memories) fashion before the athlete’s recollection of the past seems continuous. Following injury, the duration of retrograde amnesia will tend to shrink over time.57
Anterograde amnesia represents the period between the time that head injury occurs and the point at which the athlete regains continuous memory functioning for events happening following head injury. Again, this amnesia may present as solid, “spotty,” or often an initial period of relatively solid amnesia, followed by spotty amnesia, then normal continuous memory functioning. On the sideline, brief anterograde amnesia can be assessed by documenting an athlete’s ability to recall three words following a brief delay. In a clinical interview and follow-up setting, a clinician can determine through an interview the athlete’s memory functioning in the hours and days after an injury. Table 332-3 contains an example of sideline assessment questions that can be used to document retrograde and anterograde amnesia.
TABLE 332-3 Acute Mental Status Testing Protocol from the University of Pittsburgh Medical Center’s Sideline Assessment
| Orientation |
Presence of either form of amnesia because of concussion has been linked to increased neurocognitive difficulties and worse symptoms following injury.52 In this study by Collins and associates, athletes with the greatest symptomatic and neurocognitive impairment at approximately day 2 postinjury were more than 10 times more likely to have experienced retrograde amnesia because of the concussion, and 4 times more likely to have experienced anterograde amnesia, although the presence of LOC was not predictive of poor outcome.
Balance Problems
Traumatic brain injury has been known to cause benign paroxysmal positional vertigo, labyrinthine concussion, perilymphatic fistulas, central vestibular disorders, endolymphatic hydrops, and cervicogenic vertigo.58 Balance difficulties following sports-related concussion have been well-documented in the literature.38,59–61
Mildest Mild Brain Injuries or “Ding” Injuries
In sports-related mTBI, as well as other causes, such as falls or motor vehicle accidents, “ding” injuries are often left unrecognized and untreated. It has been common for decades to hear individuals say they have “shaken off” mild injuries and continued with sports or other activities. At times, such injuries are not properly addressed at emergency departments or primary care offices, only to become larger problems when the mild symptoms do not resolve and an athlete is prematurely returned to play. The athlete can sustain a more severe injury or a worsening of symptoms from the mild injury as the person attempts to re-enter work and other activities of daily living, developing symptoms of postconcussion syndrome. In a groundbreaking study examining the nature of “ding” injuries, Lovell and associates62 examined a group of concussed high school athletes who had sustained AAN grade 1 concussions (e.g., transient confusion, no LOC, resolution of symptoms, and mental status changes within 15 minutes of injury). Memory scores were significantly lower than baseline at 36 hours postinjury, but had returned to baseline levels by day 6. Although athletes had claimed symptom resolution within 15 minutes of injury during the sideline evaluation, symptom scores reflected significant increases in symptoms at the 36 hour postinjury assessment that had resolved by day 6. Of the 43 subjects in the study, only 4 exhibited both asymptomatic status and baseline-equivalent neuropsychological functioning by the 36 hour postinjury follow-up.
Consistent with findings of Lovealls study, a study examining the severity of impairment between levels of grade 1 concussions revealed cognitive and symptomatic deficits for at least 4 days postinjury.63 Furthermore, when grade 1 injuries were further divided based on injury severity (<5 minutes on-field symptoms versus 5 to 15 minutes of on-field symptoms), the less severe group (<5 minutes reported symptom duration) demonstrated increased symptom reporting at the 36-hour postinjury assessment and memory dysfunction at 4 days postinjury, while the more severe group demonstrated deficits on memory testing through the final (day 7) assessment. A study assessing sideline processing speed performance in Australian rules football43 yielded similar results, with significant differences between athletes reporting less than 5 minutes of symptoms when compared with those reporting greater than 15 minutes of symptoms.
Age Effects of Sports Concussion
The number of young athletes participating in sports continues to grow, with as many as 60% of high school students participating in organized sports.64 More than 1.5 million high school and younger athletes participate in American football alone,65 and it is estimated that up to 30 million children ages 5 to 17 participate in community sponsored athletic programs.66,67
Many animal studies have provided a solid foundation to our understanding of age-related changes following mTBI. In rat studies using fluid percussion to model mild-to-moderate concussion (little to no observable structural injury), injured rats showed reduced cognitive benefit from enriched environment rearing when compared with shams raised in the same environment up to 1 month postinjury. However, if enriched environment rearing was delayed until 2 weeks postinjury, the injured rats performed more similarly to shams, though with a slightly reduced learning slope and worse performance on a delayed memory task.68 In the absence of cell death following fluid percussion brain injuries, immature rats demonstrated mild acute cognitive deficits (e.g., slowed escape latency and delayed task learning), but no storage or recall memory difficulties.69
Human studies of age effects in mild traumatic brain injury suggest that younger age may place an injured person at greater risk for slow recovery or poor acute outcome following concussion. Many of these studies have focused on sports-related head injuries. When examining time to recover based on symptom resolution and memory performance, a college athlete’s were found to recover more quickly than high school athlete’s. Memory impairment was detected for at least 1 week postinjury in a high school sample, but recovered within 24 hours in a collegiate sample.70 High school football players were found to recover more slowly than their NFL counterparts, though both groups initially demonstrated concussion-related neurocognitive decline relative to the baseline. Most professional athletes returned to baseline within 2 days, and all returned to normal by 1 week postinjury. High school football players recovered more slowly, as evidenced by longer lasting symptoms and cognitive deficits following concussion.71 Also, the extent to which postinjury scores departed from baseline were much greater in the high school versus the professional sample. In this study, concussed high school athletes were also found to have a higher rate of RGA following concussion, but did not significantly differ on the rate of LOC or disorientation. An epidemiologic study of concussion in North Carolina high school students found that being younger (e.g., ninth grade) was a moderate predictor of concussion rate.16
Epidemiologic studies of mTBI in younger populations tend to find teenagers at greater risk for injury compared with younger children.8,72,73 Also, causes of mTBI vary among age groups. For example, one study found that collision with home furnishings and fixtures were more likely to injure children younger than 7 years of age, while sports and recreational equipment were linked to the highest frequency of mTBI in those 7 to 18 years of age.72
Research examining patients with moderate to severe traumatic brain injury suggests that developmental physiologic differences may underlie age effects. The younger brain may experience more prolonged and diffuse swelling following injury,74–77 and is significantly more sensitive to glutamate (see the pathophysiology section earlier).78 Increased vulnerability to injury in children may also be linked to developmental differences in the brain, skull, and musculoskeletal systems.79 Second impact syndrome is most often recorded in persons in their teenaged years or younger,80,81 suggesting increased vulnerability in the developing brain.
Gender Effects with mTBI
In many studies, mTBI has been documented as occurring more frequently in males.8,82,83 Despite a growing body of literature examining gender differences in recovery from mTBI, the clinical picture remains unclear. A meta-analysis examining sex differences in outcome following TBI found women performed worse than men on 85% of measured variables, with men performing worse on only auditory symptoms.84 Female gender has been associated with significantly greater endorsement of postconcussion symptoms acutely postinjury in mTBI44,85–87 and general trauma85 patients, and in symptom reporting at baseline (preinjury) testing.44
For example, a study comparing the neurocognitive and symptom reporting in concussed collegiate males and females found no difference in postinjury cognitive performance or symptom reporting at day 2 or 8 assessments. Although there were no between-subject multivariate effects of sex found in this study, univariate posthoc analyses revealed concussed females performed worse on visual memory, and concussed males more often reported higher symptom scores of sadness and vomiting. Broshek and coworkers88 found that a sample of high school and collegiate women demonstrated worse simple and complex reaction times, processing speed, and symptom scores when compared with their male counterparts. Another study of collegiate athletes participating in six sports found that women were at increased risk for sustaining a concussion during games (9.5% for women versus 6.4% for men). This same study cited women’s soccer players as having the highest concussion rate and women’s lacrosse for having the highest inherent risk for concussion during a game.89 Regarding differences in psychological responses to injury, women tend to report more concern about the impact of injury on their health, while men report more pressure to play through an injury.90
Other Influencing Factors on Response to or Recovery from mTBI
The idea of cognitive reserve has received attention for its potential role in quicker recovery from brain injury, including mTBI. Patients that score lower on IQ testing have been found more likely to experience persistent postconcussion syndrome (PCS) following brain injury,91 though those with higher IQ scores were found in one study to be more likely to endorse at least three ICD-10 postconcussion symptoms acutely (within about 5 days) following brain injury.85 A study of collegiate football players revealed that athletes with a self-reported diagnosed learning disability and a history of multiple concussions were found to perform more poorly on baseline testing than did those with a history of multiple concussions without a diagnosis of a learning disability.28
Psychiatric difficulties, both before and after brain injury, have been linked to risk of poor outcome. Acute posttraumatic stress85 and posttraumatic stress disorder (PTSD)92 have been related to high postconcussion symptom endorsement. Preinjury histories of affective or anxiety disorders85,91 and other psychiatric disorders91 have been associated with greater acute85 and persistent91 postconcussion symptoms. Ruff and colleagues93 suggested, through several case studies, that specific premorbid emotional and personality characteristics potentially place people at increased risk of poor outcome from mTBI. This “miserable minority” was characterized as being overachieving, dependent, perfectionistic, grandiose, having borderline personality characteristics, and/or narcissistic features.
