In the past decade, there has been growing public awareness and concern regarding the risk and consequences of concussion in contact sports.1 However, there has not been a corresponding increase in the ability to objectively diagnose and effectively treat concussion. At the 2010 Ice Hockey Summit I: Action on Concussion, prioritized action items included improved recognition, diagnosis, and return-to-play protocols in addition to rule changes and rule enforcement aimed at reducing head contact. The main priorities of the 2013 Ice Hockey Summit II: Action on Concussion were elimination of all hits to the head and fighting. Data presented at Summit II showed that the “uppercut” (knock out) punch has much greater forces than other on-ice hockey-related infractions.2 Unfortunately, targeting the head, fighting in games, and locker room boxing are all dangerous exposures that continue in hockey. The fighting-related data combined with lawsuits filed by players against the National Hockey League (NHL) may eventually lead to the elimination of fighting in ice hockey. Body checking,3–5 particularly when accompanied by “checking from behind,” boarding, and head hits are also dangerous, but can be addressed by rule changes6,7 as has occurred in PeeWee hockey in both Canada and the United States and high school hockey in the United States.
The potential link between head trauma and long-term neurologic deficits has increased public health concerns regarding sport-related concussion (SRC).8–11 High-impact head trauma occurs in all contact sports, such as hockey, football, and soccer, but strategies to reduce incidental and eliminate intentional head impact are essential for player safety.12–15 Hockey is played at high speeds on hard, slippery ice, surrounded by boards and Plexiglas. Consequently, SRC frequently results from body checks, accidental collisions and deliberate infractions.3–5,16–26 In hockey, the incidence of concussion and other injuries increases as players physically mature, because of increased size, speed, and their competitive aggression.12,14,27,28
Video reconstruction is a bioengineering procedure that contributes to our understanding of head trauma and impact on the brain. Video reconstruction uses 2 orthogonally positioned cameras to capture head impact events and to calculate both impact speed and head accelerations.29–31 This process has established the relationship between the magnitude of head acceleration and the severity of head injury.30 Video reconstruction output is used in finite element models (FEM). The FEM output provides acceleration magnitude, strain rates, and brain tissue orientation at the time of injury.29,31–37 These impact characteristics can be used in the translational laboratory and animal research to evaluate responses to simulated head impacts and potential therapies.
Wearable accelerometers and instrumented helmets have also been developed to measure and track head impacts and their relation to SRC. The Head Impact Telemetry System (HITS) has been used extensively to record impacts.1,2,22,26,38–41 The magnitude, frequency of head hits, and linear and rotational accelerations have been studied in both male and female hockey players, at youth, high school, Junior A and college age levels of participation.1,2,17,22,26,38,40–45
A study of Bantam players (ages 13–14 years) recorded 2753 impact events over 10 g with an average linear acceleration of 15.8 g (SD 13.8). Five players experienced >180 impacts each, with some exceeding 98 g.39 In another study of high school, Junior A, and collegiate (men's and women's) teams, over 100 000 head impacts were measured with player-to-player contact accounting for 50% of the impacts. Sport-related concussion was diagnosed most often on days with higher frequency and magnitude of recorded head impacts.43 Head impact exposure, which includes parameters of frequency, magnitude, and head impact location,2 was correlated with both concussion signs and symptoms and abnormalities on functional magnetic resonance imaging and diffusion tension imaging.46–48
High linear and rotational accelerations have been simulated in the laboratory using an HITS hockey helmet and a Hybrid III head–neck complex to study impact characteristic correlations during 3 common infractions: static cross-checking, dynamic cross-checking, and slashing to the head–neck complex.49 Mean linear accelerations ranged 26.5 g from a crosscheck to 138 g from a slash, and mean rotational accelerations ranged from 2260 rads/s2 during a dynamic cross check, to 14 100 rads/s2 during a slash.49
A 2-season study of Junior A players (N = 28) wearing HITS17,29,45 helmets at home games looked at HITS accelerations, SRC diagnosed in season (6 in 2011–2012 and 4 in 2012–2013), individual exposure time, penalties, and video data. These players reported between 0 and 6 concussions each before enrolling in the study. During the 2011 to 2012 season, 5201 impacts over 10 g were recorded and 2780 in 2012 to 2013. The number of impacts ranged between 103 and 186 per player per season and between 6.8 and 7.06 per player per game per season. There were 47 fights in the 2011 to 2012 season and 34 in the 2012 to 2013 season, based on the penalties recorded for fighting.
Highest single linear and rotational accelerations per player were graphed separately on 80% probability of the concussion scale of Zhang,50 and diagnosed concussions were marked with an X (Figure 1).51 All but one of the concussed players recorded linear and rotational accelerations above an 80% probability of concussion. However, 10 players with accelerations over the 80% probability line were not diagnosed with a concussion; was this due to impact measurement error? To answer this question, drop testing was performed with a Hybrid III Head Form fitted with an HITS hockey helmet. Results showed a strong correlation between accelerations recorded from the Hybrid III and the HITS helmet, except for drops onto the ridged vertex of the helmet. Assured by the strong correlations that the head impacts were being accurately recorded, the accuracy of the concussion diagnostic methods, including the Sport Concussion Assessment Tool 3 (SCAT3), were questioned.52–54 Other potential explanations for head hits above the 80% concussion probability levels without a diagnosis of concussion include the lack of player motivation to report head trauma, acquired resiliency to head hits, and fear of reporting consequences such as missed playing time or loss of a scholarship opportunity.
Despite technological advances that allow a quantitative evaluation of head impact that measure accelerations during games showing the magnitude and frequency of head impact events in hockey, our ability to diagnose concussion at rinkside or point of care has not advanced beyond the currently available subjective clinical assessment tools.1,2
Subjective Concussion Diagnosis Process
The currently available “objective” diagnostic tools, such as the SCAT3, are subject to players underreporting or exaggeration of symptoms. The absence of an objective, readily available and affordable quantitative measure of brain function impairs our ability to accurately assess SRC. Likewise, the inability to clinically measure the initial magnitude of neuronal injury and objectively monitor brain recovery over time weakens informed decision making for treatment, prognosis, and return to sport.1,2 The lack of objective measures for diagnosis of concussion and serial quantitative measures of recovery compromise the identification and assessment of prospective therapies. Currently, no Food and Drug Administration (FDA)-approved therapy is available for acute concussion, and treatment options are limited to rest, time, and nonpharmacologic rehabilitation strategies.
The SCAT3 has been recommended as an aid to the diagnosis of concussion.54 This test battery queries concussion history, 22 symptoms, orientation, memory, delayed recall, and balance testing. All of the SCAT3 responses are vulnerable to manipulation during baseline and postconcussion testing, if players are motivated to avoid a concussion diagnosis. Players who “cheat” the test often remain on the field of play and are subject to the risk of subsequent head trauma. Recognition, scholarships, professional contracts, or starting positions are motivation to deny symptoms. A recent review of the psychology of athletes with concussion highlights limitations of diagnosing concussions due to the subjectivity of the evaluation.55
Gaps in Current Concussion in the Hockey Literature
Clinicians are challenged by the absence of reliable objective measures to diagnose, quantify severity, and inform the management of concussion. The clinical evaluation of concussion resembles chest pain management in the 1950s. Electrocardiograms were challenging to interpret and provided only a semiquantitative measure of cardiac injury, serum biomarker assessments did not exist, and the sole treatment was rest for several weeks with comfort care, often including morphine and oxygen. A few decades later, clinicians can expediently and accurately evaluate and treat chest pain, track myocardial injury recovery, and return patients to “normal” life in a matter of days. Although the SCAT3 provides a structured assessment of the athlete's after head trauma event, more objective diagnostic protocols are emerging, which will provide much needed objectivity to the concussion evaluation.
Components of an Objective Diagnosis of Concussions
Our hockey concussion research team is investigating objective diagnostic measures that use a repeated measure design, so the players serve as their own control. The team selected 4 time points to use for measuring: (1) preseason baseline, (2) after head trauma, (3) before return to sport, and (4) after season testing.
Mayo Clinic Ice Hockey Concussion Survey
This demographic survey queries an athlete's concussion history and hockey profile (years in hockey, player position, and on-ice playing style) before segueing into the objective diagnostic measures using the King–Devick test, the quantified electroencephalogram (QEEG), and neurobiomarker measurements.
The King–Devick (KD) test, a time-based measure of saccades and other eye movements, detects concussion with high levels of sensitivity (86%) and specificity (90%) at rinkside or point of care.56 A preseason baseline is performed with players wearing practice/competition eyewear. Examiners record the time it takes to complete each of 3 trials and the number of errors per trial.56 Recently, 141 youth hockey players underwent KD testing before season, after season, and immediately after suspected concussion.57 Testing was also performed in a subgroup of nonconcussed athletes immediately before and after games to determine the impact of fatigue on KD scores. Twenty athletes sustained a concussion, and all 20 had immediate postconcussion KD testing times, which deviated more than 5 seconds from baseline (average 7.3 s) and all but 2 had worse postseason scores (46.4 seconds vs 52.4 seconds, P < 0.05). In contrast, 51 nonconcussed players assessed before and after a game revealed no significant time change as a result of fatigue. This study indicated that the KD test accurately identified real-time, symptomatic concussion in youth athletes. Players will benefit from having provided preseason and postseason KD testing, as sports medicine providers will have a real-time objective evaluation at point of care to support the diagnosis of concussion.
During a QEEG evaluation, event-related potentials (ERPs) reveal ongoing, covert neurologic processing deficits not fully assessed by behavioral measures. Event-related potentials are sensitive measures of neurofunctional deficits, which are not influenced by either player motivation or by the practice effects of repeated testing, a limitation of KD testing. A QEEG was used to assess concussed athletes between 2010 and 2012 in a repeated measure design (baseline, immediately after injury, 45 days after concussion, and before return to play). Although most SRC symptoms and cognitive dysfunction resolved within the first week after injury, QEEG results showed that postconcussion neurofunctional recovery, as measured on the QEEG, lags behind clinical recovery.58–60
Authors used the NeuroCatch (NC; NeuroTech Lab, Surrey, BC, Canada), a QEEG device, which identifies changes in waveform amplitude and latency, after head trauma compared with baseline. The NC requires 1 to 2 minutes to set up and 5 minutes to record the brain waveforms The NC allows comparison of the preseason baseline with a postinjury recording, which may aid in making a concussion diagnosis and guide the return-to-play decision.
To date, the neurobiomarker measurements of neuron-specific enolase, S100B, and Tau have yielded equivocal results for diagnosis and severity of head trauma in several studies.61–65 Two novel neurobiomarker tools recently used in hockey studies are metabolomics66–68 and αII-spectrin N-terminal fragment (SNTF).69,70 These biomarkers show promise of improved accuracy for diagnosis of SRC after head trauma in hockey. The metabolomics involves analyzing blood plasma to detect metabolite “footprints” indicative of head trauma. Metabolomic profiles have distinguished mild cognitive impairment from Alzheimer disease,67,68 and similar profiles have differentiated concussed adolescent male hockey players from nonconcussed players.66
The SNTF measurements detected axonal trauma after head injury in Swedish professional hockey players.69 Although undetectable at baseline, SNTF rises after head trauma and is used in a repeated measure design to provide a clinical profile of readiness for return to play as SNTF levels return to undetectable levels.
In future research, the goal is for these and other objective diagnostic tests to confirm concussion diagnosis, quantify severity, and contribute to the study of potential concussion treatment. Although virtually no evidence-based treatment for acute SRC is now available, evolving information on an objective diagnosis of concussion will result in a framework capable of assessing treatment efficacy. Objective and accurate concussion diagnoses in hockey players and other contact sport athletes are essential to allow for controlled, randomized trials to evaluate effects.
Treatment with Promising Medication
Treatment with medications requires understanding of the postconcussion neurometabolic cascade. This cascade is characterized by increases in intracellular glutamate and calcium, coincident with potassium exiting the intracellular space into the extracellular fluid, a chemical process that impedes phosphorylation of ATP necessary for brain energy function. Consequently, the postconcussion acute cellular energy demand exceeds the intracellular energy supply.71,72 As such, effective treatment of concussion at point of care will likely require the ability of agents that expediently cross the blood–brain barrier and promptly reduce the neurometabolic energy crisis.
To date, evidence supporting pharmacologic concussion treatment is symptom driven and equivocal in patients with postconcussion syndrome.73 Symptom categories reviewed were (1) somatic complaints, (2) sleep disturbance, (3) emotional difficulties, and (4) cognitive difficulties. Although administration of most medications is symptom driven, some agents show promise in circumventing the cell energy crisis that produces concussion symptom constellations.
In a military study performed in Iraq, a clinician administered either N-acetyl cysteine (NAC) or a placebo to combat soldiers after blast-related traumatic brain injury at point of care. N-acetyl cysteine has a 40-year history of clinical use in acetaminophen overdose without discernable side effects. Study participants were randomized into either NAC treatment (N = 41) or placebo group (N = 40), with the NAC group showing significant symptom improvement. N-acetyl cysteine has also shown neuroprotective benefits and use in treating neurological disorders; however, it does not easily cross the blood–brain barrier, which limits brain cell bioavailability.74–76 An amide derivative of NAC, NAC amide, has been synthesized that crosses the blood–brain barrier efficiently resulting in increased brain cell bioavailability. Animal model studies of N-acetylcysteine amide (NACA) show significant benefit in rodent traumatic brain injury (TBI), spinal cord injury, and focal penetrating brain injury models with no side effects. A review of NACA studies concluded that NACA may soon be available as a treatment for SRC.77 There are also some animal data supporting potential neuroprotective benefits from the use of common fish oils, such as docosahexaenoic acid,78,79 but additional research is needed to prove efficacy. It is hoped that the reported neuroprotective benefits from these promising treatments will show the ability to prevent and alleviate post-SRC symptoms in athletes to a level that will attain FDA approval.
Promising Treatment Without Medication
Recent nonpharmacologic treatment has challenged the use of complete physical and cognitive rest with prolonged activity restrictions in concussed athletes. Although relative rest is useful in the acute concussion period, exercise at a subsymptom threshold using the Balke treadmill protocol has proven benefits in postconcussion syndrome.80–85 In addition to exercise, other interventions are often necessary including oculomotor, cervical spine, and vestibular rehabilitation.86,87 Additional interventions to decrease the risk of postconcussion musculoskeletal injuries may also be necessary with some athletes.88
Considerable effort has been invested in developing a comprehensive version of the SCAT3 that includes a concussion history, extensive symptom assessment, severity rating, orientation awareness, memory and delayed recall, and a preliminary vestibular assessment; however, collectively, these evaluations remain subjective. As illustrated by investigative reports,89 many committed athletes escape concussion detection based on their motivation to remain in the game. At all levels of participation, pressure on clinical providers from coaching staff, general managers, and players can also impede the accuracy of the concussion diagnoses. As objective diagnostic tools become available, the diagnosis will be less vulnerable to subjective overlay of overly aggressive athletes and assertive coaches.
Practical Guidelines for Clinicians
Medical personnel evaluating athletes who sustain significant head impact should be aware that most currently used diagnostic tests are imprecise, require athlete cooperation, and are vulnerable to player and evaluator bias. The SCAT3, despite being well studied and widely used, consists of a series of subjective questions, or tests requiring player cooperation, and thus, is susceptible to player deception. Although psychometrics ensure validity, they do not necessarily ensure objectivity. Clinicians should use tests with the greatest objectivity, availability, and affordability.
This review provides sports medicine team physicians and athletic trainers with action(s) that can be integrated into their concussion assessment. The diagnostics discussed in this article are most helpful at this time when a baseline comparison test is available. Important information for clinicians to know before objectively diagnosing a hockey-related concussion includes risk factors such as: (1) a history of previous concussions, (2) head contact exposures along with the frequency to known accelerations at over 80% probability, and (3) the on-ice position of forward in ice hockey.
To advance the science of concussion, objective measures to diagnose concussion and document the resolution of brain-related changes must be developed. Variations from baseline in 3 objective measures—the KD test, the QEEG, and neurobiomarkers—may confirm concussion and measure of severity of the brain injury. These potential objective measures will enable promising therapeutic options to be studied for efficacy in concussion management. Using objective diagnostic methods is a critical step to reduce the frequency and consequences of undiagnosed concussion and inappropriate return to play.
The authors thank Douglas Fraser, MD, PhD (University of Western Ontario), Robert Siman, PhD (University of Pennsylvania), and Ryan D'Arcy, PhD, and his team (Sujoy Ghosh Hajra, Careesa Liu, Shaun Fickling, Gabriela Pawlowski at Simon Fraser University) for their contributions to an objective diagnosis of concussion. The authors also thank Chad Eickhoff, ATR, ATC, Kristen Greek, ATR, ATC, Eric Crowley, ATR, ATC, and Andrew Thoreson, MS, for contributing their input and insights into this project as it has evolved; and Pam Otterbein for her editorial assistance, Pat Erwin for her reference librarian skills, and the USA Hockey Foundation for partial funding support.
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