Concussion in Sport
Summary and Keywords
Concussions affect millions of athletes of all ages each year in a variety of sports. Athletes in certain sports such as American football, ice hockey, rugby, soccer, and combative sports like boxing are at higher risk for concussion. Direct or indirect mechanical forces acting on the skull and brain cause a concussion, which is a milder form of brain injury. Conventional neuroimaging (e.g., computerized tomography [CT], magnetic resonance imaging [MRI]) for concussion is typically negative. Concussions involve both neurometabolic and subtle structural damage to the brain that results in signs (e.g., loss of consciousness [LOC], amnesia, confusion), symptoms (e.g., headache, dizziness, nausea), and functional impairment (e.g., cognitive, balance, vestibular, oculomotor). Symptoms, impairment, and recovery time following concussion can last from a few days to weeks or months, based on a variety of risk factors, including younger age, female sex, history of concussion, and history of migraine. Following a concussion, athletes may experience one or more clinical profiles, including cognitive fatigue, vestibular, oculomotor, post-traumatic migraine (PTM), mood/anxiety, and/or cervical. The heterogeneous nature of concussion warrants a comprehensive approach to assessment, including a thorough clinical examination and interview; symptom inventories; and cognitive, balance, vestibular, oculomotor, and exertion-based evaluations. Targeted treatment and rehabilitation strategies including behavior management, vestibular, vision, and exertion therapies, and in some cases medication can be effective in treating the various concussion clinical profiles. Some athletes experience persistent post-concussion symptoms (PCS) and/or psychological issues (e.g., depression, anxiety) following concussion. Following appropriate treatment and rehabilitation strategies, determination of safe return to play is predicated on being symptom-free and back to normal levels of function at rest and following exertion. Certain populations, including youth athletes, may be at a higher risk for worse impairment and prolonged recovery following concussion. It has been suggested that some athletes experience long-term effects associated with concussion including chronic traumatic encephalopathy (CTE). However, additional empirical studies on the role of concussion on CTE are needed, as CTE may have multiple causes that are unrelated to sport participation and concussion.
Incidence of Concussion
The Centers for Disease Control and Prevention (CDC) estimate that in the United States alone, approximately 1.6 to 3.8 million sport-related concussions (SRC) occur annually (Langlois, Rutland-Brown, & Wald, 2006). As many as 1.9 million of these SRCs involve children under the age of 18 years (Bryan, Rowhani-Rabhar, Comstock, & Rivara, 2016). However, many SRCs go unreported, so the number of actual injuries is likely much higher (McCrea, Hammeke, Olsen, Leo, & Guskiewicz, 2004). Certain sports such as collision (e.g., American football, rugby) and contact (e.g., soccer, basketball) sports have higher rates of concussion than sports that involve limited contact. Among collegiate student athletes in the United States, men’s wrestling (10.92 concussions per 10,000 exposures), men’s ice hockey (7.91 concussions per 10,000 exposures), and women’s ice hockey (7.50 concussions per 10,000 exposures) had the highest rates of SRC (Zuckerman et al., 2015). Regarding overall numbers, this same study reported that men’s American football and women’s soccer resulted in the greatest total numbers of SRCs. Among adolescent (i.e., high school) aged athletes, rates are highest in American football for males (6.4 concussions per 10,000 exposures) and in soccer (3.4 concussions per 10,000 exposures) for females (Marar, McIlvain, Fields, & Comstock, 2012). Only a handful of studies have looked at concussions in youth (i.e., <13 years) sports, and have reported similar rates as high school aged athletes in American football (Kontos et al., 2013) and ice hockey (Kontos et al., 2016). In a recent meta-analysis of studies on SRC in youth that extended to athletes aged 18 years, researchers reported that rugby (4.18 concussions per 1000 exposures) had the highest incidence of concussion, but that overall rates (0.23 concussions per 1000 exposures) were fairly low across all sports (Pfister, Pfister, Hagel, Ghali, & Ronksley, 2016). It is presumed that athletes in sports involving speed (e.g., downhill skiing, racecar driving), acrobatic tricks (e.g., competitive cheer, snowboarding, skateboarding, surfing), and combat (e.g., boxing, mixed martial arts) are also at risk for concussion. However, data regarding the specific incidence of concussion in these sports are not available. It is important to note that concussions may occur in any sport including distance running and swimming. Therefore, although certain sports may have higher incidence of concussion, awareness of concussion among athletes, coaches, parents, and sports medicine staff is important across all sports.
Definition of Concussion
There are dozens of definitions of SRC, and the definition has evolved considerably over the past couple of decades. Earlier definitions were based primarily on loss of consciousness (LOC; e.g., Cantu, 1986), which occurs in only about 10% of concussions (Guskiewicz et al., 2006). Consequently, colloquial terms, such as “ding,” or having one’s “bell rung” were often used to refer to what we now know were concussions (Guskiewicz et al., 2004). Use of these terms is discouraged, as the term concussion as currently defined can be more broadly applied to these events. More recent definitions by expert consensus groups and professional organizations have focused on altered mental function resulting from direct or indirect trauma to the brain. For examples, the American Academy of Neurology (AAN) provides a broad definition for concussion, allowing for any trauma-induced alteration in mental state (Giza et al., 2013). Specifically, the definition states, “… concussion is recognized as a clinical syndrome of biomechanically induced alteration of brain function, typically affecting memory and orientation, which may involve LOC” (Giza et al., 2013, p. 2250). Similarly, the National Athletic Trainers’ Association defined concussion as, “a trauma induced alteration in mental status that may or may not involve loss of consciousness” (Broglio et al., 2014, p. 246). Adopting a more global and less specific definition, the American Medical Society for Sports Medicine (AMSSM) defined concussion as a “traumatically induced transient disturbance of brain function,” that “involves a complex pathophysiological process” (Harmon et al., 2013, p. 15). The most commonly used definition comes from the 4th International Conference on Concussion in Sport in Zurich (McCrory et al., 2013), which defines a concussion as, “… a complex pathophysiological process affecting the brain, induced by biomechanical forces” (McCrory et al., 2013, p. 250). The Zurich consensus statement purports there are several common factors among concussions that may be useful in defining the injury (McCrory et al., 2013). First, concussions may be caused by either a direct blow to the head or an indirect hit elsewhere on the body, resulting in an impulsive force. Second, neurological symptoms following concussions typically begin rapidly and resolve spontaneously; however in some cases, symptoms may take longer to evolve. Third, concussions my result in neuropathological changes, but more frequently, clinical symptoms are a result of a functional disturbance. However, neuroimaging almost always reveals no structural abnormalities in a concussed athlete. Finally, concussions will produce an array of graded symptoms that may or may not include LOC. Resolution of these symptoms follows a typical sequence, but in some special cases, recovery may be prolonged (McCrory et al., 2013).
Biomechanics of Concussion
For a concussion to occur, a shift in kinetic energy is required, specifically an acceleration and deceleration of the head and brain (Mihalik, 2012). Acceleration refers to a sudden speeding up of the head and brain. Typically this occurs when a stationary head is struck by a moving object, sending the head in motion (Park & Levy, 2008). Deceleration is a slowing down of the head and brain (Mihalik, 2012), which often occurs when an athlete’s moving head strikes a stationary object and comes to an abrupt stop (Park & Levy, 2008). Acceleration can be further broken down into linear and rotational acceleration. Linear acceleration is when the brain moves in a straight line, while rotational acceleration occurs when the brain moves on an arc, deviating from the brain’s center of gravity (Mihalik, 2012; Ommaya, Goldsmith, & Thibault, 2002). Rotational acceleration is thought to be more likely to result in shearing of brain tissue, causing diffuse axonal injury (Ommaya et al., 2002). While early research suggested the main cause for concussions and LOC was rotational acceleration (Ommaya & Gennarelli, 1974), more recent research surrounding concussive injuries suggests the cause is some combination of linear and rotational acceleration (Guskiewicz et al., 2007; Mihalik, Bell, Marshall, & Guskiewicz, 2007).
The forces causing acceleration can be either direct or indirect. Acceleration and deceleration results in either an impact or an impulse. An impact is a direct blow to the head, while an impulse is a force experienced elsewhere on the body that sends the head into motion (Mihalik, 2012; Ommaya et al., 2002). An example of an impact or direct force would be a helmet-to-helmet tackle in American football, where the opponent’s helmet directly contacts the athlete’s head (helmet). In contrast, an example of an impulse or indirect force would be a traditional tackle, where the opponent is stopping the athlete’s body from being in motion while the head continues in motion, resulting in the head feeling the impulse mechanism. The severity of SRC is related to the acceleration of the head and brain, as well as the impact and impulse mechanisms (Mihalik, 2012).
Pathophysiology of Concussion
After a concussive injury, a neurometabolic cascade occurs in the brain. This process involves a combination of ionic shifts, altered metabolism, and changes in neurotransmission that results in neuronal dysfunction (Giza & Hovda, 2001, 2014). The neuronal dysfunction following concussion is transient in nature and therefore quite unlikely to result in cell death. The ionic, metabolic, and physiologic events occur rapidly after injury. Immediately following a concussion, there is a release of neurotransmitters and excitatory amino acids, including glutamate, which can activate receptors responsible for potassium (K+) and calcium (CA+) exiting and entering the cell, respectively. Once these receptors are activated, there is an influx of CA+ into the cell and an efflux of K+ out of the cell. Because the cell is always striving to achieve homeostasis, the sodium-potassium (NA+-K+) pump begins to work overtime, attempting to restore previous cellular potential. In order for the NA+-K+ pump to maintain this increased workload, it requires increasing amounts of adenosine triphosphate, which boosts glucose metabolism. At this time there is also a reduction in cerebral blood flow (CBF), potentially as low as 50% of normal blood flow. As a result of the diminished CBF and the increased glucose metabolism, there is a disparity between glucose supply and demand, resulting in a significant energy crisis (Giza & Hovda, 2001, 2014). After this stage of glucose hypermetabolism, the brain then enters a period of depressed metabolism. However, prolonged increases in CA+ continue to worsen the energy crisis experienced in the brain. If the CA+ increases persist and remain unchecked, neural connectivity may be impaired. Furthermore, cell death may occur as a result of CA+ accumulations (Giza & Hovda, 2001). Another component of the pathophysiology of a concussion is the generation of lactic acid as a result of accelerated glycolysis. As previously stated, following a concussion there is a state of glucose hypermetabolism. This hypermetabolism stimulates lactate production. Lactate metabolism is concurrently decreased, resulting in an accumulation of lactate. Increased lactate levels can result in neural dysfunction and may leave neurons more vulnerable (Giza & Hovda, 2001, 2014).
Signs and Symptoms of Concussion
Athletes may present with many different signs and symptoms following a concussion. Signs are observable changes that are evident following a concussion and might include LOC, post-traumatic amnesia (PTA), confusion/disorientation, vision problems (i.e., blurry, double-vision) vomiting, numbness/tingling, balance problems, and motor incoordination (McCrory et al., 2013). Certain signs such as dizziness are indicative of longer recovery times (Lau, Kontos, Collins, Mucha, & Lovell, 2011). Typically, signs are evaluated at the time of injury by trained clinicians. In contrast, symptoms are self-reported. Among the most commonly reported symptoms following a concussion are headache, fatigue, feeling slowed down, drowsiness, difficulty concentrating, feeling mentally foggy, and dizziness (Lovell et al., 2006). Less commonly reported symptoms include nervousness, feeling more emotional, sadness, numbness or tingling, and vomiting (Lovell et al., 2006). Concussion symptoms are typically measured using self-report questionnaires, where the athlete rates their symptoms using Likert-type scales (Kontos et al., 2012). Total number of symptoms and total symptom severity scores are used to assess overall symptoms following a concussion. Concussion symptoms may also persist for several months at which point they are referred to as post-concussion symptoms or PCS (McCrory et al., 2013).
As a result of the different presentation of symptoms, researchers and clinicians have aggregated concussion symptoms into categories or factors, which can be beneficial in the treatment and management of concussions. In a study of 1,438 high school (n=944) collegiate (n= 494) athletes within a week of a concussion, Kontos and colleagues (2012) reported that there is a primary, global symptom factor—cognitive-fatigue-migraine- that includes headache, dizziness, fatigue, drowsiness, sensitivity to light/noise, feeling slowed downed, mentally foggy, and difficulty remembering/concentrating). In addition, some athletes may experience affective (i.e., sadness, nervousness, and feeling more emotional), somatic (i.e., vomiting and numbness/tingling), and sleep arousal (i.e., trouble falling asleep and sleeping less than usual) symptoms (Kontos et al., 2012). Approximately one or two weeks after injury, concussions symptoms appear to cluster into four factors that include somatic, cognitive, affective, and sleep-related symptoms (Pardini et al., 2004).
Impairment Following Concussion
In addition to signs and symptoms, athletes may experience a variety of impairments following concussion including cognitive and neuromotor, such as vestibular and oculomotor dysfunction (Broglio, Collins, Williams, Mucha, & Kontos, 2015; Collins, Kontos, Reynolds, Murawski, & Fu, 2014). Cognitive impairment following concussion may include decreased performance on memory and attention tasks, and slowed reaction time (Kontos et al., 2016). These cognitive impairments may last from a few days to several weeks following concussion (Kontos et al., 2016). Similarly, some athletes may experience problems with neuromotor function including balance, gait, vestibular, and oculomotor impairment following a concussion (Kontos & Ortega, 2011). Balance or postural stability impairment may affect athletes following concussion (Guskiewicz, 2001). However, balance impairment appears to resolve within the first days post injury (McCrea et al., 2003). Gait may also be impaired following concussion (Oldham, Munkasy, Evans, Wikstrom, & Buckley, 2016), which is particularly relevant in the sport environment. More recently, researchers have reported vestibular (e.g., vestibular ocular reflex, visual motion sensitivity) and oculomotor (e.g., smooth pursuits, saccades, convergence distance) impairment following concussion (Mucha et al., 2014). Impairments in these areas both at the time of injury and in the first weeks following injury appear to be predictive of poor outcomes (Lau et al., 2011; Womble et al., 2016).
It is generally accepted that recovery following SRC takes 7 to 14 days (McCrory et al., 2013). However, more recent research suggests that the average recovery time for high school and collegiate athletes is likely longer than previously reported (Henry, Elbins, Collins, Marchetti, & Kontos, 2016). In fact, recovery may vary from 1 week to 3–4 weeks and be domain (e.g., cognitive, symptoms, vestibular) specific (Collins et al., 2016; Henry et al., 2016). Recovery time following SRC may also vary based on a variety of factors including age, sex, concussion history, and the nature of the injury itself. Overall, younger (i.e., high school aged) athletes recover slower than older (i.e., collegiate/adult) athletes (McCrory et al., 2013). Although recent research suggests that younger adolescents take longer to recover following SRC than children (<12 years) and older adolescents (>16 years), which suggest a more curvilinear relationship between age and recovery time (Purcell et al., 2016). Females take longer to recover on average than males (Henry et al., 2016). However, recently research suggests that premorbid somatization levels may explain these sex differences (Root et al., 2016). Athletes with a history of concussion may also take longer to recover following subsequent injury (Covassin, Stearne, & Elbin, 2008). A relatively few athletes experience prolonged recovery from concussion lasting months or even years. This group, which is referred to as the “miserable minority,” may experience PCS for several months or longer (Iverson, 2006). The key to determining recovery time is to employ a multimodal approach that assesses multiple domains, as recovery may vary depending on the domain and nature of the injury and the athlete (Henry et al., 2016). In summary, recovery from concussion can vary from a few days to months, but may extend further in some athletes with certain risk factors.
Risk Factors for Poor Outcomes
Currently, there are mixed results regarding whether or not age is a risk factor for poor outcomes following concussion. Research by McCrea and colleagues (2003) exploring post-concussive symptoms, cognitive performance, and postural stability following a concussion in collegiate football players suggests the majority of athletes will be cleared for competition by 7 days post injury. Lovell and colleagues (2003) similarly explored recovery patterns from concussion in high school athletes. Contrary to the collegiate athletes studied by McCrea and colleagues, cognitive recovery had not been reached by day 7 in the high school athletes, whereas symptoms resolution had occurred by day 4 (Lovell et al., 2003). Other researchers have noted high school athletes often perform worse on neurocognitive measures following concussion (Field, Collins, Lovell, & Maroon, 2003; McClincy, Lovell, Pardini, Collins, & Spore, 2006; Moser, Schatz, & Jordan, 2005). Conversely, some studies have found no age-related differences in symptom presence and duration in high school and collegiate athletes (Lee, Odom, Zuckerman, Solomon, & Sills, 2013; Covassin et al., 2012; Meehan, Mannix, Stracciolini, Elbin, & Collins, 2013).
Exploring sex differences in outcome and recovery from concussion has shown that females tend to report more symptoms at baseline (Covassin et al., 2006; Shehata et al., 2009) and following concussion (Colvin et al., 2009; Covassin, Elbin, Harris, Parker, & Kontos, 2012) than males. Colvin and colleagues found that even when accounting for the increased baseline symptoms, females still reported more symptoms following concussion. Additionally, female athletes tend to fare worse on neurocognitive measures following concussion at both the high school and collegiate level (Broshek et al., 2005; Colvin et al., 2009; Covassin et al., 2007; Covassin et al., 2012). In fact, Broshek and colleagues found females demonstrated cognitive impairments 1.7 times more frequently than males following concussion.
Early research suggested athletes who had sustained a previous concussion within the last year reported more symptoms, and specifically experienced LOC and amnesia at a greater rate, than those players who had not incurred a previous concussion within the last year (Gerberich, Priest, Boen, Straub, & Maxwell, 1983; Guskiewicz, Weaver, Padua, & Garrett, 2000). Collins and colleagues (2002) examined the presence of on-field concussive signs in athletes with no history of concussion, compared to those with a history of 3 or more concussions, and found those athletes with a history of concussion were significantly more likely to present with on-field LOC, anterograde amnesia, and confusion after a concussion, than those athletes with no prior concussion history. Research exploring recovery time following concussive injuries noted a striking comparison between those athletes with no previous concussions and those with 3 or more previous concussions, as prolonged recovery occurred in 7.4% of athletes versus 30.0% of athletes, respectively (Guskiewicz et al., 2004). Further, research has demonstrated prolonged impairment on neurocognitive measures for those athletes with a history of multiple concussions (Covassin, Moran, & Wilhelm, 2013; Covassin et al., 2008), as well as a higher report of post-concussive symptoms (Covassin et al., 2013; Eisenberg, Andrea, Meehan, & Mannix, 2013). Eisenberg and colleagues found pediatric patients who had sustained a previous concussion within the last year had nearly 3 times the median duration of symptoms compared to those who had no previous concussion history and those who had sustained a concussion over one year prior. These findings suggest individuals with a history of multiple concussions are at an increased risk for experiencing more signs and symptoms following a concussion, as well as longer symptom duration and prolonged recovery.
Prognostic Risk Factors
Certain on-field and acute factors have shown some utility in predicting outcomes following concussion. Previous research is mixed on whether or not LOC and PTA predict poorer outcomes following concussion. Some researchers have suggested that LOC is associated with protracted recovery (Asplund, McKeag, & Olsen, 2004; McCrea et al., 2012; Pellman, Viano, Casson, Arfken, & Powell, 2004), but other researchers have not supported this relationship (Chrisman, Rivara, Schiff, Zhou, & Comstock, 2013; Guskiewicz et al., 2004; Lau et al., 2011; Makdissi et al., 2010). Similarly, while some researchers have demonstrated that athletes with PTA have a prolonged recovery (Asplund et al., 2004; McCrea et al., 2012; Pellman et al., 2004), others have supported no difference in recovery outcomes for athletes with PTA (Guskiewicz et al., 2004; Lau et al., 2009). Additionally, although the presentation of headache following SRC is not necessarily related to outcome as it is the most common symptom, prolonged headaches lasting more than a week have been reported to be associated with longer recovery time (Asplund et al., 2004; Makdissi et al., 2010). Further, headaches coupled with nausea and light and/or noise sensitivity, representing post-traumatic migraine (PTM) symptoms, have been associated with a protracted recovery following SRC (Kontos et al., 2013). When assessing acute presentation of cognitive symptoms, dizziness, drowsiness and fogginess; along with concentration, cognitive, and memory problems, all have been associated with a longer recovery time following SRC (Chrisman et al., 2013; Makdissi et al., 2010; Iverson, Gaetz, Lovell, & Collins, 2004; Lau et al., 2009, 2011). In summary, there is equivocal support for the role of LOC and PTA, but also emerging support for cognitive problems, dizziness, fogginess, PTM, and prolonged headache in regard to poor outcomes following SRC.
Conceptual Framework for SRC
Given the many different symptoms and impairments following SRC, it is somewhat surprising that until recently concussion was conceptualized, assessed, and managed from a unidimensional perspective. However, concussions involve different symptoms and impairments, and are heterogeneous. In response to this heterogeneity, researchers and clinicians have proposed clinical profile models that recognize the heterogeneity of SRC (Collins et al., 2014; Ellis, Leddy, & Willer, 2014). Ellis and colleagues (2014) suggest that SRC involves three primary disorders: (1) cervicogenic, (2) vestibulo-ocular, and (3) physiological. Collins and colleagues proposed six clinical profiles including (1) vestibular, (2) ocular-motor, (3) cognitive/fatigue, (4) post-traumatic migraine, (5) cervical, and (6) anxiety/mood (Collins et al., 2014). These approaches advocate for targeted therapies for SRC based on a comprehensive assessment.
Comprehensive Assessment of SRC
A comprehensive assessment of SRC begins with on-field or immediate post-injury measures of symptoms, mental status, cognitive function, balance, vestibular and oculomotor impairments. These assessments should be administered in a private, quiet environment (e.g., locker room, sport medicine/athletic training room) as soon as possible after a suspected concussion. Following a positive initial assessment at the time of injury, additional, more in-depth clinical assessments should be conducted in the days that follow the initial injury. The cornerstone to clinical concussion assessment is a thorough clinical interview and exam involving a personal and family medical and psychosocial history, symptom evaluation, and injury information. Athlete (or parent for youth) self-report symptom evaluations are another important component of the assessment of concussion. Among the more common symptom evaluations are the post-concussion symptom scale (PCSS) and Rivermead Post-Concussion Symptom Inventory. Computerized neurocognitive assessments such as AXON, CNS Vital Signs, and the Immediate Post-Concussion and Assessment and Cognitive Testing (ImPACT) are commonly used to assess attention, memory, and reaction time following SRC. Clinical assessments of balance such as the Balance Error Scoring System (BESS) should be performed with all athletes following a concussion. Assessments of gait including the Functional Gait Assessment (FGA; Wrisley et al., 2004) should also be employed following concussion. Impairments in vestibular and oculomotor function can be assessed using the Vestibular/Ocular-Motor Screening (VOMS; Mucha et al., 2014) tool. Finally, exertion-based assessments may be used to evaluate symptom provocation following aerobic or dynamic exertion movements that mimic the demands of specific sports. Conventional neuroimaging approaches involving computerized tomography (CT) and magnetic resonance imaging (MRI), though helpful for ruling out structural brain injury, are not effective for assessing concussion (Pulsipher, Campbell, Thoma, & King, 2011). Although there is currently no clinically accepted neuroimaging sequence for concussion, emerging findings suggest that advanced neuroimaging techniques including functional MRI (fMRI; Czerniak et al., 2015) and diffusion tensor imaging (DTI; Miles et al., 2008) may hold promise for assessing concussion. Similarly, while there are no established blood biomarkers for concussion, the combination of several markers into an assay-based approach to assessing concussion may be effective in the near future (Wang et al., 2005). The reader is referred to Papa and colleagues (Papa, Ramia, Edwards, Johnson, & Slobounov, 2015) for a systematic review of biomarkers and concussion.
Psychological Issues Following SRC
Concussion is the “invisible injury” because it is not readily evident like other injuries in sports, resulting in hidden issues associated with the injury (Bloom, Horton, McCrory, & Johnston, 2004). Consequently, psychological issues can adversely affect athletes following SRC and complicate recovery (Kontos et al., 2016). Nearly 30% of athletes report psychological symptoms following concussion (Kontos et al., 2012). Anxiety (Iverson & Lange, 2003) and depression (Kontos et al., 2012) are the most common psychological issues related to concussion and may be a direct result of a concussion or represent a psychological response to the injury. Consequently all athletes should be screened for psychological issues following SRC and referred for treatment as indicated (Kontos et al., 2016). Athletes may struggle to cope with concussion or at the very least cope differently with this injury than with orthopedic injuries (Kontos et al., 2013). Therefore, as researchers have indicated, athletes may benefit from social support following a concussion (Mainwaring, Hutchison, Bisschop, Comper, & Richards, 2010).
Treatment and Rehabilitation
Current consensus for management of SRC is initial prescribed rest with progressive return to activity based on reported symptoms (McCrory et al., 2013). However, research suggests that prescribed rest may not be effective for all patients (Thomas, Apps, Hoffmann, McCrea, & Hammeke, 2015). Therefore, concussion clinical care is moving from rest-based, passive management approaches to more active and targeted treatment approaches (Collins et al., 2016). In short, there is a paradigm shift toward the notion that the symptoms and impairments associated with concussion are treatable (Collins et al., 2016). Emerging research shows that low to moderate level physical exertion therapy may expedite recovery following concussion (Leddy et al., 2010; Leddy et al., 2016; Majerske et al., 2008). Vestibular therapies are effective for patients with these clinical profiles (Broglio, Collins, Williams, Mucha, & Kontos, 2015; Schneider et al., 2013). Vision/oculomotor therapies are also effective in treating athletes with visual problems following SRC (Broglio et al., 2015; Thiagarajan & Ciuffreda, 2014). When other therapies are not effective, athletes with certain symptoms may benefit from prescribed medications following SRC (Brody, 2014; Meehan, Taylor, & Proctor, 2011). Unfortunately, many still athletes do not receive appropriate or any care following SRC. In fact, researchers suggest that nearly 56% of SRCs do not seek care following their concussion (O’Kane et al., 2014).
Return to Play
Athletes should never return to play (RTP) on the same day as a SRC (McCrory et al., 2013). Recent evidence suggests that athletes who continue to play with SRC risk doubling their recovery time (Elbin et al., 2016) in addition to less common, but more severe and potentially fatal outcomes such as second impact syndrome (SIS). With SIS, an athlete who is still experiencing post-concussion symptoms returns to play and incurs a second, often mild impact, resulting in rapid cerebral edema and in many cases death (Cantu, 1992, 1998; Cantu & Gean, 2010; Cantu & Voy, 1995). Second impact syndrome is rare, and effects younger male athletes usually under the age of 18 years (Cantu & Gean, 2010). It is current consensus that RTP following SRC should occur only when all symptoms have resolved both at rest and following exertion (Broglio et al., 2014; Cantu, 1992; Giza et al., 2013; Harmon et al., 2013; McCrory et al., 2013). Further, RTP should occur individually in a gradual, stepwise progression (Broglio et al., 2014; Giza et al., 2013; Harmon et al., 2013; McCrory et al., 2013). In a gradual, stepwise RTP, the athlete should not progress to the next stage of exertion if they report symptoms following exertion in the current stage. However, researchers have reported that nearly 30% of athletes who were asymptomatic at rest exhibited cognitive decline (i.e., performed below baseline levels) on at least one neurocognitive test (McGrath et al., 2013). This finding suggests that reliance on symptom reporting alone following exertion protocols may result in returning some athletes to play that may still be impaired (i.e., scoring below baseline) following SRC.
Concussion in Youth Sports
As many as 1.9 million youth have a SRC each in the United States (Bryan et al., 2016). Researchers have suggested that these younger athletes may be at greater risk from SRC due to their developing brain (Field et al., 2003, McCrory et al., 2013). In addition, there are limited tools to assess concussion in younger athletes, and there is typically less medical coverage for SRC in youth sports compared to high school and collegiate sports. Among the only tools available for use in younger (i.e., 5–12-year-old) athletes are the SCAT3 Child version and Pediatric ImPACT. Researchers also suggest that concussion in children may result in higher incidence of cerebral edema (Giza & Hovda, 2001). In animal model research, younger rats that are exposure to brain injury during key developmental periods do not demonstrate subsequent similar increases in cortical thickness and cognitive performance as uninjured rats (Giza & Hovda, 2001). This finding suggests that concussion may have more pronounced effects on youth during key developmental periods such as adolescence. Purcell and colleagues (2016) have suggested that the effects of concussion are more pronounced and recovery time is longer in adolescents than in younger children. The effects of SRC in youth, particularly adolescents, warrant more attention from researchers and clinicians alike.
Other Issues Related to Concussion
Exposure to Soccer Heading
Soccer is repeatedly touted as having one of the highest rates of SRC (Cusimano et al., 2013; Gessel, Fields, Collins, Dick, & Comstock, 2007; Marar et al., 2012). Given soccer’s unique nature in that players specifically attempt to hit the ball with their heads to control play, some research has suggested soccer players may be at an increased risk for concussion. Previous research exploring the mechanism of injury in soccer players has noted heading to account for the majority of injuries (Andersen et al., 2004; Comstock, Currie, Pierpoint, Grubenhoff, & Fields, 2015; Gessel et al., 2007; Marar et al., 2012); however, the SRC is not often caused by player-to-ball contact, but rather player-to-player contact during the heading duel (Agel, Evans, Dick, Putukian, & Marshall, 2007; Andersen, Arnason, Engebretsen, & Bahr, 2004; Comstock et al., 2015; Cusimano et al., 2013; Delaney, Puni, & Rouah, 2006; Marar et al., 2012). Interestingly, Anderson and colleagues noted that often this player-to-player contact was a result of foul play. Recently, many restrictions have been made, including those made by U.S. Soccer, which limit heading exposure. A recent meta-analytic review aggregated findings from multiple studies and explored the effects of heading in soccer (Kontos et al., 2016). After reviewing the literature, no overall adverse effects on recovery outcomes from heading the soccer ball were noted. Specifically, the review found no conclusive evidence that heading is dangerous and it did not have an effect on concussion symptoms.
Chronic Traumatic Encephalopathy (CTE)
The concept of CTE, which refers to neurodegeneration associated with hyperphosphorylated tau deposits in the brain from exposure to repeated concussive or subconcussive blows to the head is not new. Researchers and clinicians have proposed these neurodegenerative effects for nearly 90 years (Solomon & Sills, 2014). Currently, CTE can only be diagnosed pathologically in the brain at death. Clinically, CTE is not well understood or characterized, but may include cognitive impairment, motor incoordination, irritability, and changes in mood (Montenigro et al., 2015). Most of what we know about CTE comes from a series of case studies of former athletes (e.g., McKee et al., 2009; Omalu, Hamilton, Kamboh, DeKosky, & Bailes, 2010). However, comorbid conditions such as psychological disorders and substance abuse were not adequately controlled for in these studies. Moreover, a link between concussion and CTE has not been supported in the literature (e.g., Hazrati et al., 2013). Additional research on CTE, from both a clinical and pathological perspective, which controls for known confounding variables is warranted.
Concussions affect millions of athletes of all ages each year; however, as many as 57% of these athletes do not receive care following SRC (Bryan et al., 2016). Collision and contact sport athletes are at higher risk for SRC, but concussions can affect athletes in any sport. In general, a concussion involves changes in brain function associated with biomechanical forces acting on the brain. Concussions occur following either direct or indirect linear and/or rotational accelerations involving the head and brain, resulting in a neurometabolic cascade in the brain. Following a SRC, athletes may experience a myriad of signs, symptoms, and impairments including cognitive, vestibular, oculomotor, and balance. Recovery time following RSC can vary from days to months or longer depending on the domain measured and an athlete’s risk factors. Athletes with a history of concussion, who are female, and who are adolescent are at greater risk for poor outcome following SRC. Additional emerging risk factors for poor outcomes following SRC include PTM, dizziness, fogginess, and prolonged headache. Concussions are heterogeneous, comprising different clinical profiles. Concussion cannot be imaged diagnostically using conventional CT and MRI, as abnormal findings are rare and usually reflect more severe injury to the brain. Instead clinicians employ a comprehensive assessment involving a thorough clinical exam/interview, and assessments of symptoms; and cognitive, vestibular, oculomotor, and balance impairment. Emerging neuroimaging—involving fMRI, DTI—and blood biomarker assessments are promising, but are not yet ready for clinical use. Following SRC some athletes experience psychological issues including anxiety and depression and should be screened and referred for treatment when appropriate. The symptoms and impairments from SRC are treatable using active targeted approaches involving vestibular, vision/oculomotor, and exertion therapies, as well as medications in certain cases. Athletes who continue to play following SRC are at increased risk for SIS and prolonged recovery. Immediate removal from play following a concussion is central to preventing these potential adverse effects. In addition, evolving RTP criteria for athletes following SRC that incorporate additional testing beyond symptom self-reports should continue to be developed. Concussions remain a concern in youth sport participants, particularly adolescents, and warrant more attention from researchers to better understand the developmental effects of this injury. Researchers will need to continue to examine the potential long-term issues related to concussion, including repetitive brain trauma and its postulated relationship with CTE. However, additional research on these topics that employs sound methodologies is needed moving forward.
Agel, J., Evans, T. A., Dick, R., Putukian, M., & Marshall, S. W. (2007). Descriptive epidemiology of collegiate men’s soccer injuries: National Collegiate Athletic Association Injury Surveillance System, 1988–1989 through 2002–2003. Journal of Athletic Training, 42(2), 270.Find this resource:
Andersen, T. E., Arnason, A., Engebretsen, L., & Bahr, R. (2004). Mechanisms of head injuries in elite football. British Journal of Sports Medicine, 38(6), 690–696.Find this resource:
Asplund, C. A., McKeag, D. B., & Olsen, C. H. (2004). Sport-related concussion: Factors associated with prolonged return to play. Clinical Journal of Sport Medicine, 14(6), 339–343.Find this resource:
Bloom, G. A., Horton, A. S., McCrory, P., & Johnston, K. M. (2004). Sport psychology and concussion: New impacts to explore. British Journal of Sports Medicine, 38(5), 519–521.Find this resource:
Brody, D. L. (2014). Concussion care manual. Oxford: Oxford University Press.Find this resource:
Broglio, S. P., Cantu, R. C., Gioia, G. A., Guskiewicz, K. M., Kutcher, J., Palm, M., & Valovich McLeod, T. C. (2014). National Athletic Trainers’ Association position statement: Management of sport concussion. Journal of Athletic Training, 49(2), 245–265.Find this resource:
Broglio, S. P., Collins, M. W., Williams, R. M., Mucha, A., & Kontos, A. P. (2015). Current and emerging rehabilitation for concussion: A review of the evidence. Clinical Journal of Sports Medicine, 34(2), 213–231.Find this resource:
Broshek, D. K., Kaushik, T., Freeman, J. R., Erlanger, D., Webbe, F., & Barth, J. T. (2005). Sex differences in outcome following sports-related concussion. Journal of Neurosurgery, 102(5), 856–863.Find this resource:
Bryan, M. A., Rowhani-Rahbar, A., Comstock, R. D., & Rivara, F. (2016). Sports-and recreation-related concussions in U.S. youth. Pediatrics, 138(1), e20154635.Find this resource:
Cantu, R. C. (1986). Guidelines for return to contact sports after a cerebral concussion. Physician and Sportsmedicine, 14, 75–83.Find this resource:
Cantu, R. C., (1992). Cerebral concussion in sport: Management and prevention. Sports Medicine, 14(1), 64–74.Find this resource:
Cantu, R. C. (1998). Second-impact syndrome. Clinics in Sports Medicine, 17(1), 37–44.Find this resource:
Cantu, R. C., & Gean, A. D. (2010). Second-impact syndrome and a small subdural hematoma: An uncommon catastrophic result of repetitive head injury with a characteristic imaging appearance. Journal of Neurotrauma, 27(9), 1557–1564.Find this resource:
Cantu, R. C., & Voy, R. (1995). Second impact syndrome: A risk in any contact sport. Physician and Sportsmedicine, 23(6), 27–34.Find this resource:
Chrisman, S. P., Rivara, F. P., Schiff, M. A., Zhou, C., & Comstock, R. D. (2013). Risk factors for concussive symptoms 1 week or longer in high school athletes. Brain Injury, 27(1), 1–9.Find this resource:
Collins, M. W., Kontos, A. P., Okonkwo, D., Almquist, J., Bailes, J., Barisa, M., et al. (2016). Statement from the Targeted Evaluation and Active Management (TEAM) Approaches to Treating Concussion Meeting in Pittsburgh, PA, October 15–16, 2015. Neurosurgery, 79(6), 912–929.Find this resource:
Collins, M. W., Kontos, A. P., Reynolds, E., Murawski, C. D., & Fu, F. H. (2014). A comprehensive, targeted approach to the clinical care of athletes following sport-related concussion. Knee Surgery, Sports Traumatology, Arthroscopy, 22(2), 235–246.Find this resource:
Collins, M. W., Lovell, M. R., Iverson, G. L., Cantu, R. C., Maroon, J. C., & Field, M. (2002). Cumulative effects of concussion in high school athletes. Neurosurgery, 51(5), 1175–1181.Find this resource:
Colvin, A. C., Mullen, J., Lovell, M. R., West, R. V. Collins, M. W., & Groh, M. (2009). The role of concussion history and gender in recovery from soccer-related concussion. The American Journal of Sports Medicine, 37(9), 1699–1704.Find this resource:
Comstock, R. D., Currie, D. W., Pierpoint, L. A., Grubenhoff, J. A., & Fields, S. K. (2015). An evidence-based discussion of heading the ball and concussions in high school soccer. JAMA Pediatrics, 169(9), 830–837.Find this resource:
Covassin, T., Elbin, R. J., Harris, W., Parker, T., & Kontos, A., (2012). The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. The American Journal of Sports Medicine, 40(6), 1303–1312.Find this resource:
Covassin, T., Moran, R., & Wilhelm, K., (2013). Concussion symptoms and neurocognitive performance of high school and college athletes who incur multiple concussions. The American Journal of Sports Medicine, 41(12), 2885–2889.Find this resource:
Covassin, T., Schatz, P., & Swanik, C. B. (2007). Sex differences in neuropsychological function and post-concussion symptoms of concussed collegiate athletes. Neurosurgery, 61(2), 345–351.Find this resource:
Covassin, T, Stearne, D, & Elbin, R. (2008). Concussion history and postconcussion neurocognitive performance and symptoms in collegiate athletes. Journal of Athletic Training, 43, 119–124.Find this resource:
Covassin, T., Swanik, C. B., Sachs, M., Kendrick, Z., Schatz, P., Zillmer, E., & Kaminaris, C. (2006). Sex differences in baseline neuropsychological function and concussion symptoms of collegiate athletes. British Journal of Sports Medicine, 40(11), 923–927.Find this resource:
Cusimano, M. D., Cho, N., Amin, K., Shirazi, M., McFaull, S. R., Do, M. T., et al. (2013). Mechanisms of team-sport-related brain injuries in children 5 to 19 years old: Opportunities for prevention. PLoS One, 8(3), e58868.Find this resource:
Czerniak, S. M., Sikoglu, E. M., Navarro, A. A. L., McCafferty, J., Eisenstock, J., Stevenson, J. H., et al. (2015). A resting state functional magnetic resonance imaging study of concussion in collegiate athletes. Brain Imaging and Behavior, 9(2), 323–332.Find this resource:
Delaney, J. S., Puni, V., & Rouah, F. (2006). Mechanisms of injury for concussions in university football, ice hockey, and soccer: A pilot study. Clinical Journal of Sport Medicine, 16(2), 162–165.Find this resource:
Eisenberg, M. A., Andrea, J., Meehan, W., & Mannix, R., 2013. Time interval between concussions and symptom duration. Pediatrics, 132(1), 8–17.Find this resource:
Elbin, R. J., Sufrinko, A., Schatz, P., French, J., Henry, L., Burkhart, S., et al. (2016). Removal from play after concussion and recovery time. Pediatrics, 138(3), e20160910.Find this resource:
Ellis, M. J., Leddy, J. J., & Willer, B. (2014). Physiological, vestibulo-ocular and cervicogenic post-concussion disorders: An evidence-based classification system with directions for treatment. Brain Injury, 1–11.Find this resource:
Field, M., Collins, M. W., Lovell, M. R., & Maroon, J., (2003). Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. Journal of Pediatrics, 142(5), 546–553.Find this resource:
Gerberich, S. G., Priest, J. D., Boen, J. R., Straub, C. P., & Maxwell, R. E. (1983). Concussion incidences and severity in secondary school varsity football players. American Journal of Public Health, 73(12), 1370–1375.Find this resource:
Gessel, L. M., Fields, S. K., Collins, C. L., Dick, R. W., & Comstock, R. D. (2007). Concussions among United States high school and collegiate athletes. Journal of Athletic Training, 42(4), 495–503.Find this resource:
Giza, C. C. & Hovda, D. A., (2001). The neurometabolic cascade of concussion. Journal of Athletic Training, 36(3), 228–235.Find this resource:
Giza, C. C., & Hovda, D. A. (2014). The new neurometabolic cascade of concussion. Neurosurgery, 75(4), S24.Find this resource:
Giza, C. C., Kutcher, J. S., Ashwal, S., Barth, J., Getchius, T. S., Gioia, G. A., et al. (2013). Summary of evidence-based guideline update: Evaluation and management of concussion in sports. Neurology, 80(24), 2250–2257.Find this resource:
Guskiewicz, K. M. (2001). Postural stability assessment following concussion: One piece of the puzzle. Clinical Journal of Sports Medicine, 11(3), 182–189.Find this resource:
Guskiewicz, K. M., Bruce, S. L., Cantu, R. C., Ferrara, M. S., Kelly, J. P., McCrea, M., et al. (2006). Research based recommendations on management of sport related concussion: Summary of the National Athletic Trainers’ Association position statement. British Journal of Sports Medicine, 40(1), 6–10.Find this resource:
Guskiewicz, K. M., Bruce, S. L., Cantu, R. C., Ferrara, M. S., Kelly, J. P., McCrea, M., et al. (2004). National Athletic Trainers’ Association position statement: Management of sport-related concussion. Journal of Athletic Training, 39(3), 280–297.Find this resource:
Guskiewicz, K. M., Bruce, S. L., Cantu, R. C., Ferrara, M. S., Kelly, J. P., McCrea, M., et al. (2006). National Athletic Trainers’ Association position statement. British Journal of Sports Medicine, 40(1), 6–10.Find this resource:
Guskiewicz, K. M., Mihalik, J. P., Shankar, V., Marshall, S. W., Crowell, D. H., Oliaro, S. M., et al. (2007). Measurement of head impacts in collegiate football players: Relationship between head impact biomechanics and acute clinical outcome after concussion. Neurosurgery, 61(6), 1244–1252.Find this resource:
Guskiewicz, K. M., Weaver, N. L., Padua, D. A., & Garrett Jr., W. E. (2000). Epidemiology of concussion in collegiate and high school football players. American Journal of Sports Medicine, 28(5), 643–650.Find this resource:
Harmon, K. G., Drezner, J. A., Gammons, M., Guskiewicz, K. M., Halstead, M., Herring, S. A., et al. (2013). American Medical society for Sports Medicine position statement: Concussion in sport. British Journal of Sports Medicine, 47(1), 15–26.Find this resource:
Hazrati, L. N., Tartaglia, M. C., Diamandis, P., Davis, K. D., Green, R. E., Wennberg, R., et al. (2013). Absence of chronic traumatic encephalopathy in retired football players with multiple concussions and neurological symptomatology. Frontiers in Human Neuroscience, 7, 222.Find this resource:
Henry, L. C., Elbin, R. J., Collins, M. W., Marchetti, G., & Kontos, A. P. (2016). Examining recovery trajectories after sport-related concussion with a multimodal clinical assessment approach. Neurosurgery, 78(2), 232–241.Find this resource:
Iverson, G. L., Brooks, B. L., Lovell, M. R., & Collins, M. W. (2006). No cumulative effects for one or two previous concussions. British Journal of Sports Medicine, 40(1), 72–75.Find this resource:
Iverson, G. L., Gaetz, M., Lovell, M. R., & Collins, M. W. (2004). Cumulative effects of concussion in amateur athletes. Brain Injury, 18(5), 433–443.Find this resource:
Iverson, G. L., & Lange, R. T. (2003). Examination of “postconcussion-like” symptoms in a healthy sample. Applied Neuropsychology, 10(3), 137–144.Find this resource:
Kontos, A. P., Elbin, R. J., Fazio-Sumrock, V. C., Burkhart, S., Swindell, H., Maroon, J., & Collins, M. W. (2013). Incidence of sports-related concussion among youth football players aged 8–12 years. Journal of Pediatrics, 163(3), 717–720.Find this resource:
Kontos, A. P., Elbin, R. J., Lau, B., Simensky, S., Freund, B., French, J., & Collins, M. W. (2013). Posttraumatic migraine as a predictor of recovery and cognitive impairment after sport-related concussion. American Journal of Sports Medicine, 41(7), 1497–1504.Find this resource:
Kontos, A. P., Elbin, R. J., Schatz, P., Covassin, T., Henry, L., Pardini, J., & Collins, M. W. (2012). A revised factor structure for the post-concussion symptom scale: Baseline and postconcussion factors. American Journal of Sports Medicine, 40(10), 2375–2384.Find this resource:
Kontos, A. P., Elbin, R. J., Sufrinko, A., Dakan, S., Bookwalter, K., Price, A., et al. (2016). Incidence of concussion in youth ice hockey players. Pediatrics, 137(2), e20151633.Find this resource:
Kontos, A. P., McAllister-Deitrick, J., & Reynolds, E. (2016). Mental health implications and consequences following sport-related concussion. British Journal of Sports Medicine, 50(3), 139–140.Find this resource:
Kontos, A., & Ortega, J. (2011). Neuromotor effects of concussion: A biobehavioral model handbook of sport neuropsychology (1st ed.). New York: Springer Publishing.Find this resource:
Kontos, A. P., Sufrinko, A., Elbin, R. J., Puskar, A., & Collins, M. W. (2016). Reliability and associated risk factors for performance on the vestibular/ocular motor screening (VOMS) tool in healthy collegiate athletes. The American Journal of Sports Medicine, 44(6), 1400–1406.Find this resource:
Langlois, J. A., Rutland-Brown, W., & Wald, M. M. (2006). The epidemiology and impact of traumatic brain injury: A brief overview. Journal of Head Trauma Rehabilitation, 21(5), 375–378.Find this resource:
Lau, B. C., Kontos, A. P., Collins, C. L., Mucha, A., & Lovell, M. R. (2011). Which on- field signs and symptoms predict protracted recovery from sport-related concussion among high school football players? American Journal of Sports Medicine, 39(11), 2311–2318.Find this resource:
Lau, B. C., Lovell, M. R., Collins, M. W., & Pardini, J. (2009). Neurocognitive and symptom predictors of recovery in high school athletes. Clinical Journal of Sport Medicine, 19(3), 216–221.Find this resource:
Leddy, J. J., Baker, J. G., & Willer, B. (2016). Active rehabilitation of concussion and post-concussion syndrome. Physical Medicine and Rehabilitation Clinics of North America, 27(2), 437–454.Find this resource:
Leddy, J. J., Kozlowski, K., Donnelly, J. P., Pendergast, D. R., Epstein, L. H., & Willer, B. (2010). A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clinical Journal of Sport Medicine, 20(1), 21–27.Find this resource:
Lee, Y. M., Odom, M. J., Zuckerman, S. L., Solomon, G. S., & Sills, A. K., (2013). Does age affect symptom recovery after sports-related concussion? A study of high school and college athletes. Journal of Neurosurgery Pediatrics, 12(6), 537–544.Find this resource:
Lovell, M. R., Collins, M. W., Iverson, G. L., Field, M., Maroon, J. C., Cantu, R., et al. (2003). Recovery from mild concussion in high school athletes. Journal of Neurosurgery, 98(2), 296–301.Find this resource:
Lovell, M. R., Iverson, G. L., Collins, M. W., Podell, K., Johnston, K. M., Pardini, D., et al. (2006). Measurement of symptoms following sports-related concussion: Reliability and normative data for the post-concussion scale. Applied Neuropsychology, 13(3), 166–174.Find this resource:
Mainwaring, L. M., Hutchison, M., Bisschop, S. M., Comper, P., & Richards, D. W. (2010). Emotional response to sport concussion compared to ACL injury. Brain Injury, 24(4), 589–597.Find this resource:
Majerske, C. W., Mihalik, J. P., Ren, D., Collins, M. W., Reddy, C. C., Lovell, M. R., & Wagner, A. K. (2008). Concussion in sports: Postconcussive activity levels, symptoms, and neurocognitive performance. Journal of Athletic Training, 43(3), 265–274.Find this resource:
Makdissi, M., Darby, D., Maruff, P., Ugoni, A., Brukner, P., & McCrory, P. R. (2010). Natural history of concussion in sport: Markers of severity and implications for management. American Journal of Sports Medicine, 38(3), 464–471.Find this resource:
Marar, M., McIlvain, N. M., Fields, S. K., & Comstock, R. D. (2012). Epidemiology of concussions among United States high school athletes in 20 sports. The American Journal of Sports Medicine, 40(4), 747–755.Find this resource:
McClincy, M. P., Lovell, M. R., Pardini, J., Collins, M. W., & Spore, M. K., (2006). Recovery from sports concussion in high school and collegiate athletes. Brain Injury, 20(1), 33–39.Find this resource:
McCrea, M., Guskiewicz, K. M., Marshall, S. W., Barr, W., Randolph, C., Cantu, R. C., et al. (2003). Acute effects and recovery time following concussion in collegiate football players: The NCAA Concussion Study. Journal of the American Medical Association, 290(19), 2556–2563.Find this resource:
McCrea, M., Guskiewicz, K. M., Randolph, C., Barr, W. B., Hammeke, T. A., Marshall, S. W., et al. (2012). Incidence, clinical course, and predictors of prolonged recovery time following sport-related concussion in high school and college athletes. Journal of the International Neuropsychological Society, 2012(18), 1–12.Find this resource:
McCrea, M., Hammeke, T., Olsen, G., Leo, P., & Guskiewicz, K. (2004). Unreported concussion in high school football players: Implications for prevention. Clinical Journal of Sport Medicine, 14(1), 13–17.Find this resource:
McCrory, P., Meeuwisse, W. H., Aubry, M., Cantu, B., Dvorak, J., Echemendia, R. J., et al. (2013). Consensus statement on concussion in sport: The 4th International Conference on Concussion in Sport held in Zurich, November 2012. British Journal of Sports Medicine, 47(5), 250–258.Find this resource:
McGrath, N., Dinn, W. M., Collins, M. W., Lovell, M. R., Elbin, R. J., & Kontos, A. P. (2013). Post-exertion neurocognitive test failure among student-athletes following concussion. Brain Injury, 27(1), 103–113.Find this resource:
McKee, A. C., Cantu, R. C., Nowinski, C. J., Hedley-Whyte, E. T., Gavett, B. E., Budson, A. E., et al. (2009). Chronic traumatic encephalopathy in athletes: Progressive tauopathy after repetitive head injury. Journal of Neuropathology & Experimental Neurology, 68(7), 709–735.Find this resource:
Meehan, W. P., Taylor, A. M., & Proctor, M. (2011). The pediatric athlete: Younger athletes with sport-related concussion. Clinics in Sports Medicine, 30(1), 133–144.Find this resource:
Meehan III, W. P., Mannix, R. C., Stracciolini, A., Elbin, R. J., & Collins, M. W. (2013). Symptom severity predicts prolonged recovery after sport-related concussion, but age and amnesia do not. The Journal of Pediatrics, 163(3), 721–725.Find this resource:
Mihalik, J. P. (2012). Biomechanics of sports concussion. In M. W. Kirkwood & K. O. Yates (Eds.), Mild traumatic brain injury in children and adolescents (pp. 38–52). New York: Guilford.Find this resource:
Mihalik, J. P., Bell, D. R., Marshall, S. W., & Guskiewicz, K. M. (2007). Measurement of head impacts in collegiate football players: An investigation of positional and event-type differences. Neurosurgery, 61(6), 1229–1235.Find this resource:
Miles, L., Grossman, R. I., Johnson, G., Babb, J. S., Diller, L., & Inglese, M. (2008). Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Injury, 22(2), 115–122.Find this resource:
Montenigro, P. H., Bernick, C., & Cantu, R. C. (2015). Clinical features of repetitive traumatic brain injury and chronic traumatic encephalopathy. Brain Pathology, 25(3), 304–317.Find this resource:
Moser, R. S., Schatz, P., & Jordan, B. D., (2005). Prolonged effects of concussion in high school athletes. Neurosurgery, 57(2), 300–306.Find this resource:
Mucha, A., Collins, M. W., Elbin, R. J., Furman, J. M., Troutman-Enseki, C., DeWolf, R. M., et al. (2014). A brief vestibular/ocular motor screening (VOMS) assessment to evaluate concussions preliminary findings. The American Journal of Sports Medicine, 0363546514543775.Find this resource:
O’Kane, J. W., Spieker, A., Levy, M. R., Neradilek, M., Polissar, N. L., & Schiff, M. A. (2014). Concussion among female middle school soccer players. JAMA Pediatrics, 168(3), 258–264.Find this resource:
Oldham, J. R., Munkasy, B. A., Evans, K. M., Wikstrom, E. A., & Buckley, T. A. (2016). Altered dynamic postural control during gait termination following concussion. Gait Posture, 49, 437–442.Find this resource:
Omalu, B. I., Hamilton, R. L., Kamboh, M. I., DeKosky, S. T., & Bailes, J. (2010). Chronic traumatic encephalopathy (CTE) in a National Football League player: Case report and emerging medicolegal practice questions. Journal of Forensic Nursing, 6(1), 40–46.Find this resource:
Ommaya, A. K., & Gennarelli, T. A. (1974). Cerebral concussion and traumatic unconsciousness: Correlation of experimental and clinical observations of blunt head injuries. Brain, 97(4), 633–654.Find this resource:
Ommaya, A. K., Goldsmith, W., & Thibault, L., (2002). Biomechanics and neuropathology of adult and paediatric head injury. British Journal of Neurosurgery, 16(3), 220–242.Find this resource:
Papa, L., Ramia, M. M., Edwards, D., Johnson, B. D., & Slobounov, S. M. (2015). Systematic review of clinical studies examining biomarkers of brain injury in athletes after sports-related concussion. Journal of Neurotrauma, 32(10), 661–673.Find this resource:
Pardini, J., Stump, J. E., Lovell, M., Collins, M. W., Moritz, K., & Fu, F. H. (2004). The Post Concussion Symptom Scale (PCSS): A factor analysis [abstract]. The British Journal of Sports Medicine, 38, 661–662.Find this resource:
Park, M. S., & Levy, M. L. (2008). Biomechanical aspects of sports-related head injuries. Neurologic Clinics, 26(1), 33–43.Find this resource:
Pellman, E. J., Viano, D. C., Casson, I. R., Arfken, C., & Powell, J. (2004). Concussion in professional football: Injuries involving 7 or more days out—Part 5. Neurosurgery, 55(5), 1100–1119.Find this resource:
Pfister, T., Pfister, K., Hagel, B., Ghali, W. A., & Ronksley, P. E. (2016). The incidence of concussion in youth sports: A systematic review and meta-analysis. British Journal of Sports Medicine, 50(5), 292–297.Find this resource:
Pulsipher, D. T., Campbell, R. A., Thoma, R., & King, J. H. (2011). A critical review of neuroimaging applications in sports concussion. Current Sports Medicine Reports, 10(1), 14–20.Find this resource:
Purcell, L., Harvey, J., & Seabrook, J. A. (2016). Patterns of recovery following sport-related concussion in children and adolescents. Clinical Pediatrics (Phila), 55(5), 452–458.Find this resource:
Root, J. M., Zuckerbraun, N. S., Wang, L., Winger, D. G., Brent, D., Kontos, A., & Hickey, R. W. (2016). History of somatization is associated with prolonged recovery from concussion. The Journal of Pediatrics, 174, 39–44.e1.Find this resource:
Schneider, K. J., Iverson, G. L., Emery, C. A., McCrory, P., Herring, S. A., & Meeuwisse, W. H. (2013). The effects of rest and treatment following sport-related concussion: A systematic review of the literature. British Journal of Sports Medicine, 47(5), 304–307.Find this resource:
Shehata, N., Wiley, J. P., Richea, S., Benson, B. W., Duits, L., & Meeuwisse, W. H. (2009). Sport concussion assessment tool: Baseline values for varsity collision sport athletes. British Journal of Sports Medicine, 43(10), 730–734.Find this resource:
Solomon, G. S., & Sills, A. (2014). Chronic traumatic encephalopathy and the availability cascade. Physician and Sportsmedicine, 42(3), 26–31.Find this resource:
Thiagarajan, P., & Ciuffreda, K. J. (2014). Versional eye tracking in mild traumatic brain injury (mTBI): Effects of oculomotor training (OMT). Brain Injury, 28(7), 930–943.Find this resource:
Thomas, D. G., Apps, J. N., Hoffmann, R. G., McCrea, M., & Hammeke, T. (2015). Benefits of strict rest after acute concussion: A randomized controlled trial. Pediatrics, 135(2), 213–223.Find this resource:
Wang, K. K., Ottens, A. K., Liu, M. C., Lewis, S. B., Meegan, C., Oli, M. W., et al. (2005). Proteomic identification of biomarkers of traumatic brain injury. Expert Review of Proteomics, 2(4), 603–614.Find this resource:
Womble, M. N., Reynolds, E., Schatz, P., Shah, K. M., & Kontos, A. P. (2016). Test-retest reliability of computerized neurocognitive testing across in youth ice hockey players. Archives of Clinical Neuropsychology, 31(4), 305–312.Find this resource:
Wrisley, D. M., Marchetti, G. F., Kuharsky, D. K., Whitney, S. L. (2004). Reliability, internal consistency, and validity of data obtained with the functional gait assessment. Physical Therapy, 84(10), 906–18.Find this resource:
Zuckerman, S. L., Kerr, Z. Y., Yengo-Kahn, A., Wasserman, E., Covassin, T., & Solomon, G. S. (2015). Epidemiology of sports-related concussion in NCAA athletes from 2009–2010 to 2013–2014 incidence, recurrence, and mechanisms. The American Journal of sports Medicine, 43(11), 2654–2662.Find this resource: