Numerous definitions have been proposed for the clinical entity known as concussion. The 2016 Berlin Consensus Statement on Concussion in Sport defined concussion as a “traumatic brain injury induced by biomechanical forces,” but notably considered concussion and mild traumatic brain injury (TBI) to be separate entities.1 In contrast, the 2013 American Academy of Neurology guidelines for sports concussion did not separate concussion from mild TBI, defining concussion as “a clinical syndrome of biomechanically induced alteration of brain function, typically affecting memory and orientation, which may involve loss of consciousness.”2
Regardless of the precise definition, an increased awareness of concussions and their potential long-term detrimental effects has led to a surge in their recognition, particularly among individuals participating in sports. The Centers for Disease Control and Prevention currently estimates that between 1.6 and 3.8 million sports-related concussions occur annually—a dramatic increase from the 300,000 concussions reported in 1996.3–5 Concussions are common in young athletes, accounting for an estimated 1.1 to 1.9 million injuries annually6 and representing approximately 8.9% of all high school sports injuries.7 Although these numbers may seem high, the actual numbers are likely higher than this owing to the combination of a lack of awareness among clinicians and a reluctance to report symptoms among athletes.8–10 The number of documented concussions is expected to continue to rise with increased participation of youth in sports and improved concussion awareness and management.11
Mechanism and Presentation
The primary mechanisms of injury are a combination of direct blow to the head and acceleration/deceleration.12 The dynamic and multivariable nature of contact sports competition makes for various possible iterations of concussive impacts. One study using game video analysis to determine the location of helmet impact in the National Football League reported that among 174 cases of impact, 29% involved loading of the facemask, with the remainder involving the helmet shell.13 For the cases involving the helmet shell, 22% involved the ground and 50% involved the other player's helmet. When both facemask and helmet shell impacts were combined in the total sample, 61% of the impacts involved the other player's helmet.
Currently, there are no approved biomarkers for diagnosing a concussion. Thus, diagnosis remains largely clinical. Further, presentations and outcomes can be highly variable both between and within individuals, making clinical assessment and prognosis exceedingly challenging.14–16 Acute symptoms may include confusion, headache, nausea and vomiting, dizziness, sensitivity to light or noise, fatigue, deficits in concentration or memory, sleep disturbance, dynamic visuomotor synchronization decline, visual disturbance (notably blurred vision), and emotional lability.12,17,18 Most patients clinically recover within weeks; however, symptom duration can be highly variable and does not offer a reliable early predictor of ultimate outcome.12,18,19 Although a single sports-related concussion is unlikely to result in long-term adverse outcomes,17,19 some patients can experience symptoms for many years, and athletes with recurrent concussions may experience longer-term effects.12 These long-term sequelae include epilepsy, neurodegeneration, Alzheimer's disease, Parkinson's disease, Lewy body disease, amyotrophic lateral sclerosis, and chronic traumatic encephalopathy.12,20–22 Since 2004, a series of reports involving individuals with exposure to repetitive brain injury have led to potential concerns about chronic traumatic encephalopathy and the heterogeneous onset of associated neurodegenerative disease, including amyotrophic lateral sclerosis, Parkinson's disease, Lewy body disease, and Alzheimer's disease.23,24
There has been a significant effort to educate both patients and clinicians about the risks, recognition, and prevention of concussions.1,8,17,25 By possessing a thorough understanding of the pathophysiology, diagnosis, and management of concussions, orthopedic surgeons can work in concert with other physicians, athletic trainers, and physical therapists to provide complete care to athletes with these injuries.11
The diagnosis of concussion presents a challenge to providers covering sports teams at any level of competition. Symptoms and signs are often nonspecific, lack objectivity, can be highly variable, and may resolve within 24 hours of injury. Rates of headache and loss of consciousness associated with concussion have been reported as 86% and 8.9%, respectively.26 The diagnosis and management of concussions are further complicated by athletes who lack education and awareness and are incentivized to return to play prior to full recovery. Given the lack of gold standard diagnostic tools and the high variability of presentation between individuals, this is a growing area of research.
Four tools for identifying individuals with concussion have been validated via studies with different levels of evidence.
Neuropsychological testing, whether on paper or on computer, was shown via a class II study27 and multiple class III studies3,28–31 to be useful in identifying the presence of concussion (71% to 88% sensitivity) in adolescents and adults. However, the evidence is insufficient to generalize these findings to preadolescents. Among the more useful neuropsychological tests, which incorporate Maddocks questions and the Standardized Assessment of Concussion, are the Sport Concussion Assessment Tool 5th Edition (SCAT5) and/or the Child SCAT5. Regarding the SCAT5, the 2016 Concussion in Sport Group consensus statement recommended its use as a rapid screening tool for sideline assessment of those suspected of having a sports-related concussion and noted that it “currently represents the most well-established and rigorously developed instrument available for sideline assessment” and is “useful immediately after injury in differentiating concussed from nonconcussed athletes, but its utility appears to decrease significantly 3 to 5 days after injury.”1
The Post-Concussion Symptom Scale and the Graded Symptom Checklist have been shown by multiple class III studies to accurately identify concussion among athletes involved in events during which biomechanical forces are imparted to the head, having 64% to 89% sensitivity and 91% to 100% specificity.28,29,32–38
The Standardized Assessment of Concussion had a lower threshold in multiple class III studies, with evidence suggesting that it is likely to identify the presence of concussion in the early stages after injury (80% to 94% sensitivity and 76% to 91% specificity).28,29,39–43
To date, the Balance Error Scoring System and the Sensory Organization Test have been shown to have low to moderate diagnostic accuracy in class III studies, with 34% to 64% sensitivity and 91% specificity for the Balance Error Scoring System28,29,44,45 and 48% to 61% sensitivity and 85% to 90% specificity for the Sensory Organization Test.3,44–46
In the future, the use of these tools in combination with early class III studies28,29,35,36 may improve the accuracy of diagnosing concussion. However, elucidating which combinations are most effective for cohorts at different stages of brain development and with different severity of symptoms will require further investigation.
Currently, the SCAT5 is considered the standard of care in sideline assessment of concussion and is the most widely used in international athletics, including in the National Hockey League, the National Basketball Association, the National Football League, and Major League Baseball.47 The Berlin consensus statement1 encourages free distribution and use of the SCAT5, which is available at http://bjsm.bmj.com/content/bjsports/51/11/851.full.pdf. The SCAT5 is not a standalone assessment tool for concussion, but rather one component of a comprehensive evaluation that, depending on the overt extent of injury, extends from airway, breathing, and circulation to a thorough physical examination ruling out acute cervical spine or other serious musculoskeletal injury to serial cognitive assessment. The SCAT5 should be performed in a quiet, distraction-free environment, such as a locker room or office, in the acute post-injury time frame to assess for changes that may indicate significant brain injury. The setting should remain constant if possible to avoid environmental contamination of scoring, which can be substantial.47
In addition to concussion detection, use of these tools for concussion prognosis and prediction of impairment after concussion has also garnered much research interest, with likely associations being found between the early period after concussion and lower Standardized Assessment of Concussion score,28,29 reduction in neuropsychological testing scores,33,48 and deficits on the Balance Error Scoring System,29 the Sensory Organization Test,37,46 and gait stability dual-task testing.26 Visual tracking (ie, eye movement, such as the King–Devick test) technology has recently evolved, and computerized versions of simpler, older assessments, such as the Immediate Post-Concussion Assessment and Cognitive Testing, have become available.49–53
Treatment is an Evolving Process
Strategies for treating concussion continue to evolve as understanding of the potential long-term negative effects of concussion increases. Although 80% to 90% of concussions symptomatically resolve within 2 weeks, some patients may have underlying ongoing processes with potentially long-term effects.54 Concussions are heterogeneous injuries that require treatment protocols tailored to individual patients' particular deficits and symptoms. Minimizing stimuli while emphasizing physical and cognitive rest have long been considered the mainstays of treatment after concussion. Although this remains true for the first 24 to 48 hours after concussion, recent studies have shown that prolonged rest may lead to symptoms of fatigue, depression, and/or deconditioning; thus, prolonged rest does not appear to be of benefit.55–57 Guidelines have changed. The Zurich Concussion in Sport Group consensus statement recommended a stepwise return-to-play protocol that has since been widely adopted. Athletes progress through a graded 6-level program that is essentially symptom driven, and they must be symptom free for 24 hours before graduating to the next level, which mandates a minimum 1 week off from athletics.11 Critical to prognosis and the likelihood of biopsychosocial dysfunction are athletes' premorbid history and baseline factors.24,58,59 There are no Food and Drug Administration–approved or evidence-based pharmacological treatments for concussion, although physicians often treat concussed athletes symptomatically.60,61 In addition to a stepwise return-to-play protocol, return-to-learning protocols are also being widely implemented. A sudden return to full cognitive activities can trigger concussion symptoms and slow the recovery process. Return-to-learning programs are especially important for student athletes.62–64 Active rehabilitation programs after sports-related concussion may be particularly beneficial for children or young adults with persistent symptoms, with a combination of cervical and vestibular physiotherapy being among the most preliminarily effective modalities.65–68
The 20% (or greater) of concussed athletes who do not recover within a few weeks of their injury represent an extremely challenging patient population for orthopedists and concussion specialists alike.69,70 Some patients may have symptoms for months or even years, whereas others will have resolution of primary symptoms but continue to exhibit a post-concussion spectrum of secondary symptoms. Referral to an experienced concussion specialist should be considered in these circumstances. Multiple alternate therapies are available, including cognitive behavioral therapy for the development of secondary symptoms, and subsymptomatic threshold exercise programs, which have recently been shown to be beneficial to recovery.71–73 Vestibular and ocular as well as cervicovestibular therapy and testing has also become more widespread as a result of apparent effectiveness in aiding recovery.68 A 2010 study examining vestibular rehabilitation for post-concussion patients with dizziness and balance issues showed that those who followed the therapy had improvement in all gait and balance performance measures.74
The Concussion “Protocol”
In general, there are many accepted return-to-play guidelines, with most being at least partially based on the 2016 Berlin Concussion in Sport Group consensus statement (Tables 1–2).1,75,76
National Football League Head, Neck and Spine Committee's Concussion Diagnosis and Management Protocol: 2017–2018 Season
National Collegiate Athletic Association Sport Science Institute Concussion Safety Protocol Interassociation Consensus: Diagnosis and Management of Sport-Related Concussion Best Practices
Potential Predisposition to Other Injuries
As discussed previously, sports-related concussion can be assessed using a variety of tests that measure postural control, neurocognitive function, and symptoms reported by the athlete. The literature has indicated that most concussed athletes show clinical resolution of symptoms, cognitive abnormalities, and balance impairment within 7 to 10 days of concussion.29,77,78 However, there is a growing body of literature supporting the notion of abnormalities in motor and brain function long after patients appear clinically asymptomatic, particularly in the neurometabolic and physiologic domains.79–82 Several studies have reported attention and mental performance deficits in asymptomatic athletes. Therefore, the diagnosis of concussion may be associated with motor issues and changes such as an adoption of a conservative gait strategy in athletes.83 In addition, other studies have suggested impaired neuromuscular control in otherwise asymptomatic athletes after concussion. This has led to emerging literature regarding whether prior concussion places athletes at increased risk of orthopedic injury despite a seemingly “full” recovery. Brooks et al84 studied 75 Division I athletes who had sustained a concussion, tracking the occurrence of noncontact lower extremity injury within a 90-day return-to-sport window. Each athlete was compared with up to 3 controls. The concussed athletes were 2.48 times more likely to sustain a noncontact lower extremity injury within their 90-day return to play than the nonconcussed athletes, a finding that achieved statistical significance.84 In a similar study, Herman et al85 examined 90 concussed Division I athletes who were matched to controls according to sport, starting status, and position. Herman et al reviewed a 90-day in-season period for time-loss to injury, finding that concussed athletes were 3.39 times more likely to sustain a lower extremity musculoskeletal injury (P<.01). The same phenomenon was studied by Lynall et al,86 who examined rates of lower extremity injury in concussed high school athletes across 27 different sports. They found that the concussed athletes were statistically significantly more likely to sustain a time-loss lower extremity injury than their nonconcussed counterparts. In a recent review of 32 different studies, Howell et al87 found evidence supporting that previously concussed athletes were at greater risk for lower extremity injury, and that dual-task neuromuscular control deficits may continue to exist in asymptomatic, previously concussed athletes. As knowledge surrounding the pathophysiology of concussion continues to grow, it is possible that the orthopedic care of the previously concussed athlete will change dramatically regarding potential for future injury. Recent data from the National Collegiate Athletic Association and Department of Defense Grand Alliance: Concussion Awareness, Research, and Education Consortium suggest that early reporting of sports-related concussion may be associated with athletes' returning to play sooner, and that ensuring brain safety may help to ensure musculoskeletal safety.88
Concussion litigation continues to be a hot topic in sports medicine. This is due, at least in part, to recent high-profile lawsuits involving professional athletes and leagues, increasing public awareness of chronic traumatic encephalopathy, and publicized stories with devastating outcomes attributed to repetitive concussions.89 As a result of the 2009 Lystedt case, concussion legislation is now active in all 50 states and the District of Columbia.90 In this case, a player who sustained a head to ground injury during a football game at which no medical staff were present to perform an evaluation continued to play despite exhibiting confusion and memory difficulty and ultimately needing life-saving emergency surgery that left him severely disabled.91 This tragedy became a landmark case that resulted in the aforementioned legislation, which is essentially based off of a 3-legged system: concussion education, removal of the athlete from play at the suspicion of injury with no allowance for return to play that day, and examination by a qualified health care professional. Orthopedic surgeons often serve as team physicians; thus, they can be thrust into the role of removing an injured or concussed athlete from competition. It is recommended that orthopedic surgeons become familiar with the concussion legislation of the state in which they practice and keep up-to-date with changes to this legislation. It is also highly advisable that all initial and serial examination be documented. It is recommended that, even if an athlete is determined not to have been concussed and is cleared to return to play, the ongoing sideline observation be documented. The standard of care of concussion will likely continue to evolve along with the understanding of the pathophysiology of concussion, as it is enhanced by biological and physiologic metric supplementation.
Development of Diagnostic Tools
In recent years, research efforts regarding the diagnosis of concussion have sought to reassess the viability of established diagnostic tools in an effort to find more rapidly deployable tools that may potentially better inform return-to-play decision making. For example, the National Collegiate Athletic Association and Department of Defense Grand Alliance: Concussion Awareness, Research, and Education Consortium conducted a 30-site investigation, involving 4874 participants, of the 6-month natural history of concussion.92 Testing of annual administrations of common and emerging concussion assessment tools, with the SCAT and Brief Symptom Inventory-18 among them, for test–retest reliability found less than optimal reliability. This study emphasized the need to account for variance in normal performance with accurately calculated confidence intervals and to test measures to thoroughly know at which time intervals their sensitivity, specificity, and/or reliability fall below levels of clinical utility. The search for new, more readily administered diagnostic tools has worked toward minimizing subjectivity and developing novel neurophysiologic measures, neuroimaging techniques, vision and oculomotor assessment, and biomarker screenings, yielding mixed results.
Neuroimaging techniques offer a minimally invasive approach with results that can be interpreted remotely. Uncinate fasciculus magnetic resonance diffusion imaging has been shown to be able to differentiate retired athletes with histories of concussion from healthy controls with 79% to 84% sensitivity and specificity.93 Pathophysiologic changes in the brain after concussion are detectable using advanced magnetic resonance imaging methods, including diffusion tensor imaging, which can detect axonal tearing, susceptibility-weighted imaging or angiography, which depict iron deposits in brain microvessels, and diffusion-weighted imaging, capable of visualizing hyper- or hypoperfusion.94 However, some magnetic resonance studies have found an unclear link to phenotype.95 Use of these neuroimaging methods in combination, such as in the case of a study employing susceptibility-weighted imaging, diffusion tensor imaging, and magnetic resonance imaging that was able to find abnormalities in 80% of patients with mild TBI, might be how they will be most effective in the future.96,97 Understanding the baseline genotypic and phenotypic factors present in a population that may leave individuals more or less susceptible to increased effects from sports-related concussions or predisposed to prolonged symptoms is important. Autonomic assessment may have a role in populations at risk of sports-related concussion and screening for autonomic dysfunction via avascular response, which would represent a relevant, clinically important phenotype.98,99
The advent of oculomotor assessment has led to, for example, the King– Devick test, which is based on rapid number naming and has been shown to accurately identify real-time, asymptomatic concussion in youth athletes.50 However, a review study examining 27 studies investigating the King–Devick test concluded that it is currently best used as a sideline screening tool, requiring further study in a broader range of patients to be used as a tool for diagnosing concussion.50 Vestibular/ocular motor screening is another proposed oculomotor assessment that, despite good preliminary internal consistency as well as sensitivity being reported, needs further validation.100–102
Research regarding biomarkers for identifying concussion has produced a few viable candidates that screen for neurotoxicity with clinically relevant levels of sensitivity and specificity, including alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid103 (89% to 91% sensitivity and 91% to 92% specificity), a peptide associated with diffuse axonal injury, NMDA104 (83% sensitivity and 91% specificity), a peptide indicative of microvessel damage at the blood–brain barrier and that correlates with development of cortical vasogenic edema, and kainite receptor105 (83% to 90% sensitivity and 83% to 92% specificity), a peptide that might be associated with brainstem injury and that regulates venous circulation and development of cytotoxic edema.94 However, these are all limited by the need for the data to be assessed within 24 hours after concussion.94 The ideal biomarker would readily cross the blood–brain barrier and be measurable in blood. Many studies have pursued this line of research and have identified potential blood biomarkers for concussion, with the most highly characterized being S100ß, a protein that regulates intracellular calcium levels in neurons and glia, neuron-specific enolase, which participates in axonal transport, glial fibrillary acidic protein, an intermediate filament protein in astrocytes, and tau, an axon-localized microtubule binding protein.97 Specifically, plasma level of hypophosphorylated tau and P-tau– T-tau ratio may outperform T-tau level as diagnostic and prognostic biomarkers for acute TBI, and they show more robust and sustained elevations among patients with chronic TBI as well.106 A recent study investigating a blood panel for detection of concussion found 4 candidate biomarkers: copeptin, galectin-3, matrix metalloproteinase-9, and occludin.107 A 3.4-fold decrease in plasma concentration of copeptin and a 3.6- to 4.5-fold increase in galectin-3, matrix metalloproteinase-9, and occludin were found in patients with mild TBI within 8 hours after injury compared with uninjured controls.107 Levels of at least 2 biomarkers were altered beyond their respective cut-off values in 90% of patients with mild TBI but in none of the uninjured controls.107 Serum neurofilament light protein, found in long white-matter axons, may serve as a suitable biomarker for neuronal damage in blood samples from patients with TBI. It has also shown promise for measured levels being able to distinguish patients with severe TBI from controls, correlating with clinical outcome variables, distinguishing survivors from nonsurvivors, and correlating with Glasgow Outcome Scale score at 12-month follow-up.108
Unfortunately, almost none of these biomarkers have reached the level of clinical use. The Food and Drug Administration recently reviewed the Brain Trauma Indicator developed by Banyan Biomarkers, Inc and authorized it for marketing in fewer than 6 months as part of its Breakthrough Devices Program. The Brain Trauma Indicator tests blood for glial fibrillary acidic protein and ubiquitin carboxy-terminal hydrolase L1, a highly neuron-specific protein that hydrolyzes small C-terminal adducts of ubiquitin. Earlier studies found that glial fibrillary acidic protein performed consistently in detecting mild to moderate TBI, computed tomography lesions, and neurosurgical intervention across 7 days, and that ubiquitin carboxy-terminal hydrolase L1 performed best in the early postinjury period.109,110 In its evaluation, the Food and Drug Administration reviewed data from a multicenter, prospective clinical study of 1947 individual blood sample screening results compared with computed tomography scan results from adults with suspected mild TBI/concussion.111 The Brain Trauma Indicator was able to predict the presence of intracranial lesions on a computed tomography scan 97.5% of the time and those who did not have intracranial lesions on a computed tomography scan 99.6% of the time.112 However, its utility may currently be limited for concussion and the strongest for defining those with complicated mild TBI.
Development of Treatment Approaches
In addition to concussion diagnostics being an area with ample opportunity for innovation and research, strategies for concussion treatment are also important. As previously discussed, there is currently little evidence supporting the role of medications in the treatment of acute concussion. Further, many common medications, such as nonsteroidal anti-inflammatory drugs or aspirin, are best avoided immediately after suspected head injury because of potential for increased risk of intracranial bleeding. Currently, medication is mostly used to manage prolonged concussion symptoms, such as difficulty concentrating, headache, sleep disturbance, and depression. The only real consensus among sports governing bodies and professional medical associations/societies is that a stepwise, graduated process for return to play after concussion is the recommended approach and that athletes with a history of multiple concussions and persistent impairment should be counseled about risk factors for developing permanent impairments with continued play. Recent research with a growing body of strong preclinical evidence and clinical experience has pointed to omega-3 fatty acid supplementation possibly being beneficial after concussion and even prophylactically.113
It is clear that concussion is a complex, variable, and common injury that is not entirely understood in terms of patho-physiology and treatment.1–5 The orthopedist's role in the spectrum of concussion management is equally murky. However, the existing literature does provide a basis on which the orthopedist who is likely to be exposed to concussed patients should operate. In the acute setting, an understanding of the multitude of mechanisms by which concussions can occur and a high index of suspicion are a must.12,13 Without exception, athletes with suspected concussions must be removed from the field of play. It is highly recommended that orthopedists have a thorough understanding of and familiarity with a sideline concussion assessment tool, such as the SCAT5. Serial assessment and the recording of each assessment are important from both a clinical and a medicolegal standpoint.1,47,90 Although there is some debate,114 baseline testing has also been shown to be beneficial for later diagnosis and treatment and should be implemented where possible.115,116 The emphasis on concussions and their sequelae in recent years must not distract the orthopedist from performing a thorough physical examination for concomitant injury. A working knowledge of post-concussion protocol, and when or if to employ concussion specialists or ancillary treatments such as cognitive behavioral therapy, is also recommended.68,72,73,98 Perhaps most important is understanding the concept that concussions vary from one individual to the next. Although individuals may exhibit similar or identical symptoms, tailored treatment is required, especially as more is learned about the cognitive impact of concussions.55–57,62–64 Also important is the realization that several studies have shown that asymptomatic athletes with concussion histories have higher rates of future lower extremity orthopedic injury; therefore, additional thorough neuromuscular testing of these athletes well into the post-concussion time period may become common.84–86 The orthopedist must keep up-to-date with the rapid developments in the biomedical and biotechnical components of diagnosis and treatment of concussion. The vestibular/ocular motor screening, imaging techniques, and biomarkers mentioned in this article represent the leading edge of a massive wave of impending literature. Given the above, combined with the legal exposure that orthopedists involved with concussed athletes face, orthopedists must be aware of changing standards of care in diagnosis and treatment going forward. Regardless of what the future holds for the management of concussion, education, timely injury reporting, new preventive measures, targeted, personalized treatment, and multidisciplinary care delivery teams will play a pivotal role in improving outcomes for these patients.117
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National Football League Head, Neck and Spine Committee's Concussion Diagnosis and Management Protocol: 2017–2018 Seasona
|No set time frame
All return to full participation decisions are confirmed by the independent neurological consultant
Step 1: Rest and recovery
Step 2: Light aerobic exercise
Stationary bike or treadmill
Supervised by the team's athletic trainer
Step 3: Continued aerobic exercise and introduction of strength training
Changing direction drills, cone drills
Continued team athletic trainer supervision
Step 4: Football-specific activities
Participation in all noncontact activities for the typical duration of a full practice
Step 5: Full football activity/clearance
Full participation in practice and contact without restriction
Step 6: Final clearance by the independent neurological consultant
National Collegiate Athletic Association Sport Science Institute Concussion Safety Protocol Interassociation Consensus: Diagnosis and Management of Sport-Related Concussion Best Practicesa
|Return-to-play management plan that specifies:|
| Final determination of return to play is from the team physician or medically qualified physician designee|
| Each student-athlete with a concussion must undergo a supervised stepwise progression management plan by a health care provider with expertise in concussion that specifies:|
| Student-athlete has limited physical and cognitive activity until he/she has returned to baseline, then progresses with each step below without worsening or new symptoms:|
| Light aerobic exercise without resistance training|
| Sport-specific exercise and activity without head impact|
| Noncontact practice with progressive resistance training|
| Unrestricted training|
| Return to competition|