Concussion in Sport

Preparation for the care of athletes begins prior to any practice or competition with a preparticipation physical evaluation (PPE) and the development and practice of an emergency action plan. The PPE should include history of concussion or other traumatic brain injury (number, recovery course and time between injuries), as well as the presence of other premorbid/comorbid conditions, or modifiers, that may make the diagnosis or management of concussion more difficult, including a history of learning disorder, attention deficit disorder, motion sickness or sensitivity, mood disorders or a personal or family history of migraine headache disorder, and information on current medication use.

Several organisations recommend baseline evaluation prior to sports participation to assist with diagnosis and return-to-play decisions in an athlete with a suspected concussion. Several factors require consideration before implementing any test into an evaluation programme for baseline or postinjury purposes. There is considerable normal variation in test performance with repeat testing in non-injured athletes; some tests are associated with a cost, and in younger athletes with rapidly developing brain function both the ideal interval to repeat baseline testing and age-related differences in test performance are unknown. Common baseline evaluations include the battery of standard sideline assessment tests found in the Sports Concussion Assessment Tool Fifth Edition (SCAT5) and/or computerised proprietary neuropsychological tests such as CogSport, Automated Neuropsychological Assessment Metrics, Central Nervous System Vital Signs, or the Immediate Post- Concussion Assessment and Cognitive Testing. An initial baseline evaluation including a symptom checklist, cognitive evaluation and balance assessment has been considered ‘best practice’ for all athletes by the National Collegiate Athletic Association. However, repeat annual baseline testing after an initial baseline evaluation is no longer recommended for collegiate athletes. Baseline testing may be useful in some cases but is not necessary, required or an accepted standard of care for the appropriate management of SRC.

Observation of athletes during practice and competition by medical personnel is valuable for potential concussion recognition and initial management. Reasons for immediate removal and prompt evaluation include loss of consciousness (LOC), impact seizure, tonic posturing, gross motor instability, confusion or amnesia. Any of these reported or observed signs should result in removal from practice or competition for at least the rest of the day. Concerns for more serious head injury including prolonged LOC, severe or worsening headache, repeated emesis, declining mental status, focal neurological deficit or suspicion of significant cervical spine injury should trigger activation of the emergency action plan.

Along with directly observed signs of potential concussion, if video review demonstrates findings such as LOC, motor incoordination or balance problems, or having a blank or vacant look, the athlete should be immediately removed from participation for evaluation. A healthcare professional familiar with the athlete is best suited to detect subtle changes in the athlete’s personality or test performance that may suggest concussion. If a concussion is suspected but not diagnosed, removal from play and serial evaluations are recommended.38 Concussion assessment should be performed in a distraction-free environment with adequate time for examination and administration of concussion tests. If it is clear an athlete has an SRC, additional sideline testing can be discontinued. Sport-specific rules may not allow adequate time for evaluation, and modifying these rules remains an area for improvement within the governing bodies of some sports.

When the sports medicine clinician becomes aware of a potential injury, the athlete is approached and a brief history of the event is obtained from the athlete and those who witnessed the event or athlete behaviour. How the athlete responds to the elements of orientation, memory, concentration and balance is evaluated, as well as speech patterns and how the athlete appears to be processing information. Cervical palpation and range of motion (ROM) are also typically performed to assess for other injury. If SRC is suspected, these preliminary evaluations are followed by a thorough and specific concussion assessment.

The psychometric properties of sideline assessment tools need to be understood to accurately interpret the results. Knowledge of test reliability, or the stability of a test administered on more than one occasion, can assist in differentiating SRC changes from normal variation. The test–retest reliability of commonly used sideline concussion evaluation tests is below the generally accepted threshold for clinical utility (0.75–0.90). Many concussion tests have a learning effect that must be factored into analysis with repeated administration of the test. The sensitivity (ability of a test to correctly identify a condition) and specificity (ability of a test to correctly identify those without a condition) of many of the individual tests used to evaluate concussion are not ideal. The area under the curve of a receiver operator characteristic curve is another way to evaluate the usefulness of a test, with values greater than 0.9 considered excellent, 0.8 good, 0.7 fair, 0.6 poor and 0.5 failing. outlines the psychometric properties and the number of subjects and concussions studied of commonly used sideline evaluation tools. There is evidence that combining tests of different functions to form a multimodal assessment increases sensitivity and specificity for diagnosis. The age of the athlete needs to be considered when using and evaluating testing tools. SRC is a heterogeneous injury which contributes to the varied sensitivity of screening tools, which are often domain-specific assessments. All tests should be interpreted in combination with relevant clinical information to arrive at the most accurate conclusion.

Symptoms are the most sensitive indicator of concussion. The reliability of athlete-reported symptoms depends on accurate reporting, which may be affected by a lack of recognition of the signs and symptoms of concussion or conscious false reporting to avoid loss of playing time. An athlete experiencing any increase in symptoms after a suspected concussion should be held from play until further evaluation can confirm or exclude SRC.

The SCAT5 and the Child SCAT5 are the evaluation tools recommended by the Concussion in Sport Group (CISG) for assessing a suspected concussion. These tests offer a standardised approach to sideline evaluation which incorporates multiple domains of function and are widely available at no cost. The SCAT5 comprised a brief neurological examination, a symptom checklist, a brief cognitive assessment (the Standardized Assessment of Concussion [SAC]) and a balance assessment (the modified-Balance Error Scoring System). The SAC in the SCAT5 offers optional 10- word lists for immediate and delayed memory and longer digit backwards sequencing to minimise the ceiling effect, which was a weakness of the SCAT3. There are currently no studies of the SCAT5 or Child SCAT5’s sensitivity and specificity for SRC to determine if these versions are improved over the earlier versions.

The primary endpoint for sideline assessment is to determine the probability that an athlete has sustained a concussion. If the athlete is deemed unlikely to have had a concussion, continued participation should be safe. If the evaluation indicates a definite or probable concussion, the athlete should be removed from participation with no same-day return to play. SRC is an evolving injury and should be serially reassessed when suspected.

An office assessment should include a comprehensive history and neurological examination including details of injury mechanism, symptom trajectory, neurocognitive functioning, sleep/wake disturbance, ocular function, vestibular function, gait, balance and a cervical spine exam. The utility of sideline neurocognitive and balance assessments to identify concussion decreases as early as 3 days after injury. Symptom checklists can be useful to track symptom trajectory. To confirm the diagnosis of SRC, there should typically be a clear mechanism consistent with concussion; characteristic signs, symptoms and time course of concussion; and no other cause for the constellation of clinical findings. It is not unusual for symptoms, signs and testing to normalise by the time an office visit occurs, in which case the visit should focus on recommendations for safe return to school and sport.

If an athlete has ongoing symptoms at the time of the first office visit, the visit should focus on excluding other pathologies and providing anticipatory guidance. Other pathologies like cervicogenic pain, headache/migraine disorder, mood disorders and peripheral vestibular conditions may either be the cause of symptoms or may represent previous pathology worsened or unmasked by concussion. A complete cervical spine evaluation, screenings for psychosocial or mental health disorders, and additional tests evaluating the vestibular and oculomotor system may be helpful in the office setting to determine the aetiology of symptoms. Vestibular symptoms occur in 67%–77% and ocular impairment occurs in approximately 45% of SRC. The Vestibular/Ocular Motor Screening (VOMS) tool offers a brief, standardised way to assess vestibular-ocular function that can be used in athletes older than 10 years of age. It is a no-cost evaluation of symptom provocation with smooth pursuits, saccades, the vestibular ocular reflex, vestibular motion sensitivity and convergence distance.

Current impact sensor systems indirectly monitor linear and angular acceleration forces to the brain; however, they may not consistently record head impacts or forces transmitted to the brain. Neither a device nor a specific threshold measure of force or angular acceleration can be used to diagnose concussion. Some athletes experience high forces with no clinical symptoms of concussion, and some athletes sustain a concussion at much lower impact forces, making current impact measures a poor predictor of SRC. The number, location, density and individual thresholds of head impacts may be important parameters. At this time impact monitors are a research tool requiring additional study and are not validated for clinical use in the diagnosis or management of SRC.

Head CT is rarely necessary in the evaluation of SRC but should be used when clinical suspicion for intracranial bleeding or macrostructural injury exists. Intracranial bleeds are rare in the context of SRC, but can occur, and CT is the standard evaluation tool for these and other suspected neurosurgical emergencies in acute and critical care. Conventional brain MRI is not commonly used in the evaluation of concussion, but may have value in cases with atypical or prolonged recovery. Newer, advanced multimodal MRI technologies (eg, diffusion tensor imaging, resting-state functional MRI, quantitative susceptibility imaging, magnetic resonance spectroscopy, arterial spin labelling) are being studied in research protocols aimed at understanding the neurobiological effects and recovery after SRC. Additional research will be required to determine the clinical utility of advanced neuroimaging in the setting of SRC.

The role of fluid biomarkers (blood, saliva, cerebrospinal fluid) in the diagnosis of SRC is also under active investigation.Proteomic markers of injury and recovery in more severe forms of civilian neurotrauma and traumatic brain injury have shown some promise. However, in recent systematic reviews, the overall level of evidence is low for using fluid biomarkers for diagnosis of SRC.50 Fluid biomarkers have potential for informing the pathophysiology of concussion and neurobiological recovery, but more research is required to determine their clinical utility. Recent Federal Drug Administration (FDA) approval of a two-protein brain trauma indicator with glial fibrillar acidic protein and ubiquitin carboxy- terminal hydrolase L1, and clinical use of S100 calcium-binding protein β in Europe, shows promise for ruling out intracranial bleeds and structural damage to reduce utilisation of head CTs in the emergency department setting. At this time, none of these tests has a role in the diagnosis or management of SRC.

There is currently no scientific support for genetic testing in the evaluation and management of athletes with SRC, and additional research is needed to determine how genetic factors influence risk of injury and recovery after SRC.

The recognition of heterogeneity among concussion presentations has led to the concept of ‘clinical profiles’ or ‘clinical domains’ with the potential for more specific prognostic value and targeted treatment. It must be stressed that this is an emerging concept and does not represent clinical standards or norms but may serve to facilitate individualised patient management. Although SRC may present with symptoms representing only one clinical profile, it is more often that SRC presents with symptoms and impairment supporting multiple profiles. It is currently unknown at what postinjury time point these profiles become clinically important as most SRCs resolve with time. Thus, clinical profiles may be more applicable to athletes with persistent symptoms. More research in this area is needed. The diverse symptoms and functional impairments of SRC are variously categorised with overlapping symptom clinical profiles that may include cognitive, affective (anxiety/mood), fatigue, migraine/headache, vestibular and ocular. How clinical profiles fit into the clinical care of SRC warrants additional research.

The most consistent predictor of recovery from concussion is the number and severity of acute and subacute symptoms. Subacute headache and depression after injury are risk factors for symptoms persisting for >1 month. A preinjury history of mental health problems, particularly depression, appears to increase the risk for prolonged symptoms. Athletes with learning disabilities or attention deficit/hyperactivity disorder do not appear to be at risk for prolonged recovery. More research is needed to address other SRC modifiers, including age and sex, although some studies demonstrate a longer period of reported symptoms in women compared with men and for adolescent athletes. Newer research suggests that a lower symptom-limited heart rate threshold during graded exercise testing within a week of SRC in adolescents predicts a longer recovery time.

Prescribed cognitive and physical rest has been the mainstay of treatment for the last several decades despite insufficient evidence to support this approach. Earlier animal data suggested that uncontrolled or forced early exercise is detrimental to recovery. However, recent data in aerobically trained animals given early access to exercise showed improved outcomes compared with no or delayed exercise or to social isolation. In human studies, strict rest after SRC slowed recovery and led to an increased chance of prolonged symptoms. Total rest, that is, ‘the dark room’ or ‘cocoon therapy’, may have detrimental effects similar to social isolation effects seen in animal studies and is no longer recommended. Consensus guidelines endorse 24–48 hours of symptom-limited cognitive and physical rest followed by a gradual increase in activity, staying below symptom-exacerbation thresholds. Further research is needed to define the role of prescribed rest in recovery.

Exercise intolerance is an objective physiological sign of acute concussion that appears to reflect impaired autonomic function and control of cerebral blood flow. Exercise improves autonomic nervous system balance and CO₂ sensitivity, cerebral blood flow regulation, brain-derived neurotrophic factor gene upregulation, and both mood and sleep. Emerging data suggest that symptom- limited activity, including activities of daily living and non-contact aerobic exercise, may begin as soon as tolerated after an initial brief period (24–48 hours) of cognitive and physical relative rest. There is some preliminary evidence that subsymptom threshold exercise improves recovery in acute concussion, and early symptom-limited graded exercise testing appears to be safe in athletes. Understanding for whom and when to begin early exercise after SRC remains an ongoing area of exploration. Early activity and exercise do not take the place of a graded return to sport.

Interest in nutraceuticals for prevention and treatment of concussion is high. There is emerging evidence in animal models of concussion that some supplements may protect or speed recovery from concussion, specifically focused on certain B vitamins, omega-3 fatty acids, vitamin D, progesterone, N-Methyl-D-aspartate, exogenous ketones and dietary manipulations (eg, ketogenic diet). There is a gap, however, between experimentally produced injury in an animal model and the heterogeneous mechanisms that cause human concussion during sports activities. There is no human evidence that nutraceuticals prevent or ameliorate concussion in athletes. Supplements are not FDA-regulated and potential for harm or contamination should be considered. This is an area that requires significantly more research to guide future recommendations.

Activity and exercise that do not exacerbate symptoms are recommended for those with persistent postconcussive symptoms. A formal symptom-limited aerobic exercise programme has been shown to be safe and improve resolution of persistent symptoms compared with controls and should be considered in athletes with symptoms lasting longer than expected. The Buffalo Concussion Exercise Treatment Protocol, a progressive subsymptom threshold aerobic exercise programme based on systematically establishing the level of exercise tolerance on the Buffalo Concussion Treadmill Test, is the most studied controlled exercise programme. It is ideal for those with persistent postconcussive symptoms to be evaluated by a provider or multidisciplinary team with expertise in complicated concussion management.

Athletes with migraine/headache should be evaluated for underlying headache disorders, cervical dysfunction causing headache and other possible contributors, and treated appropriately with non pharmacological and pharmacological treatments. Vestibular therapy should focus on specific deficits identified and use an ‘expose-recover’ model performed by clinicians with expertise in vestibular rehabilitation. There is preliminary evidence that addressing cervical spine and/or vestibular dysfunction with a targeted physical therapy programme improves outcomes in those with PPCS. Cognitive work should be modified or limited to that which does not exacerbate symptoms. In athletes with sleep disturbances following SRC, sleep hygiene should be addressed, sleep monitored and treated with non-pharmacological or pharmacological strategies. Individuals experiencing psychological symptoms such as irritability, sadness and anxiety should be evaluated and offered appropriate treatment. A collaborative care model including cognitive behavioural therapy can improve outcomes in those with persistent postconcussive symptoms.

SRC can induce changes in attention, cognitive processing speed, learning, short-term memory and executive function that make learning difficult. Return to learn is the process of transitioning back to the classroom following concussion using individualised academic adjustments. School personnel should be informed of the injury and implement an initial school support plan without delay. Many concussed athletes recover quickly enough to return to the classroom with no or very brief adjustment of academic activities, but schools should be prepared to provide additional support in the event that recovery takes longer. Athletes with persisting symptoms should be provided an individualised return to learn accommodation plan that allows for symptom-limited learning activity similar to return to physical activity protocols. Early introduction of symptom-limited physical activity is appropriate; however, return to sport training activities should follow a successful return to the classroom for student-athletes.

Concussion-related symptoms and signs should be resolved before returning to sport. A return-to-play progression involves a gradual, stepwise increase in physical demands and sport-specific activities without return of symptoms before the final introduction of exposure to contact. The athlete should also demonstrate psychological readiness for returning to play. The return-to-sport progression is individualised and is a function of the injury, the athlete’s age, prior SRC and level of play, and the ability to provide close supervision during the return to activity. The return-to-sport progression presented by the CISG is widely accepted but empiric, without evidence to support either the progression sequence or the time spent in each stage. In general, for young athletes, each stage of the progression should be at least 24 hours without return of symptoms before progressing to the next stage.

In addition to return to learning and sporting environments, older athletes may need to return to driving, where subtle deficits could compromise safety. Most sports medicine physicians do not counsel athletes with SRC about driving. Driving is a complex process involving coordination of cognitive, visual and motor skills, as well as concentration, attention, visual perception, insight and memory, which can all be affected by SRC. Little is known about the risk of driving after SRC, but preliminary data suggest some impairment exists when patients with concussion report they are asymptomatic. Currently, no widely accepted return to driving protocols exist; however, in athletes who drive, discussing the potential risks and harms is appropriate.

Continuing to play immediately following a concussion is a risk for increased symptom burden, worsening of the injury and prolonged recovery. Athletes who return to sport prior to full recovery are at increased risk of repeat concussion. Some research has demonstrated that athletes who return to sport after SRC following standard return to sport protocols had an increased rate of musculoskeletal injury. The ‘Second Impact Syndrome’ is both rare and controversial. It is considered by some to be a potentially life-threatening complication of reinjury during the initial postinjury time period that is not fully understood and appears primarily limited to paediatric and adolescent athletes.

Sport and exercise are protective against depression. Most studies examining the relationship of contact sports to mental health problems or depression later in life have low methodological quality, high risk of bias or both. Several studies have reported that NFL and college football athletes with a history of concussion are more likely to experience depression, although the risk of mental health issues, including suicide, among former NFL players is lower than age-matched controls. Former high school football players show no difference in cognitive function testing and have lower depression scores when compared with non-contact sport controls. Mental health issues are common, multifactorial and often present independent of participation in contact or collision sport. Longitudinal research on contact sport athletes that addresses multiple variables is needed to understand the long-term risks.

Chronic traumatic encephalopathy (CTE) and other neurodegenerative diseases have been described in former athletes with a history of concussion or repetitive head impact exposure, typically accompanied by behavioural change. The incidence and prevalence of CTE in the general population, in former athletes, or in former athletes with a history of concussion or repetitive head impact exposure, are unknown. A cause and effect relationship between postmortem CTE changes and antemortem behavioural and cognitive manifestations has not been demonstrated, and asymptomatic players have had confirmed CTE pathology at autopsy. It is also unknown if CTE is a progressive disease, and whether tau deposition is the cause of CTE or a byproduct or marker of a disease.

The expression of CTE-associated symptoms may be related to impact load and type, duration of career, underlying genetic factors, or other lifestyle behaviours including alcohol, drug and anabolic steroid use, general health, psychiatric disease, and other factors. Some retrospective studies have reported increased risk of neurodegenerative disease in former professional football players; however, former high school football players do not show a higher prevalence of neurodegenerative disease when compared with nonfootball peers The most widely described risk factor to date is extensive exposure to both multiple concussions and repetitive head impacts, but the degree of necessary exposure is likely specific to the individual and subject to multiple modifying risk factors. Athletes and former athletes who present with neuropsychiatric symptoms and signs that have been ascribed to CTE should be evaluated for potentially treatable comorbid conditions that share symptoms, and not be assumed to have CTE.

Subconcussive or non-concussive head impacts have been discussed as an entity apart from concussion history that may create risk of long-term neurological sequelae. Subconcussive impacts are defined as transfer of mechanical energy to the brain causing presumed axonal or neuronal injury in the absence of clinical signs or symptoms. It is unclear if a biomechanical threshold or other factors lead to injury or if this entity qualifies as injury since it does not seem to be associated with neuropsychological changes. Although subconcussive impacts have been associated with CTE, the short-term and long-term effects of repetitive head impacts, similar to SRC, cannot be accurately characterised using current technology. Future research will depend on developing technologies that can assess brain changes following repetitive asymptomatic head trauma in living subjects.

Prevention of SRC is ultimately more effective in reducing the burden of this condition than any treatment, and while primary prevention of all SRC is not possible measures to decrease the number and severity of concussions are of value. Rule changes, enforcement of existing rules, technique changes, neck strengthening and equipment modifications have been the primary focus of prevention. There is moderate evidence that delaying the introduction of body checking in youth hockey reduces concussion rates. he effectiveness of rule changes in youth soccer and football to reduce concussion incidence is not clear; however, there is initial evidence that practice modification and changes in tackling technique may reduce injury. There is conflicting evidence regarding mouthguards and concussion reduction, and mouthguards should primarily be used for preventing dental trauma. Helmets prevent skull trauma and intracranial bleeding, but their protective effects for concussion are less pronounced. Some football helmet designs have improved the ability to absorb force, but it is unknown if this will reduce concussion incidence. Studies of headgear in other sports have produced mixed results. Player behaviour can change when athletes wear new or ‘improved’ protective equipment, encouraging a more aggressive style of play, potentially increasing the risk for injury.