Ice hockey is a collision sport played at high speed on a hard surface with rigid boards. The risk of concussion has been well documented (1–7), and potential sequelae, including chronic traumatic encephalopathy (CTE), is alarming (8–13). The Ice Hockey Summit III: Action on Concussion brought together physicians, researchers, athletic trainers, sports scientists, and engineers to describe sport-related concussion (SRC) epidemiology, classify prevention strategies, define objective, diagnostic tests, identify treatment, and integrate science and clinical care into prioritized action plans and policy. Presentations and discussion panels were organized to address the objectives before attendees selected the most highly prioritized action items. The purpose of this narrative is to share the information and propose strategies to reduce the risk, severity, and consequences of concussion in the sport of ice hockey, similar to Ice Hockey Summits I and II (1–4,14,15).
Objective 1 — To Address Epidemiology and Psychosocial Influences on Concussion
Concussion susceptibility is influenced by intrinsic and extrinsic risk factor interactions. Modifiable intrinsic behaviors include balance/proprioception, physical conditioning, and psychosocial and physical health status, whereas changeable extrinsic factors include rules, equipment, training volume, and coaching. Risk factors should be considered before prevention programs are designed. Hockey, popular worldwide, currently has the following player participation and national percentages: Canada, 631,295 (1.8% of population); United States, 555,935 (0.17%); Czech Republic, 113,425 (1%); Russia, 105,059 (0.07%); Finland, 76,387 (1.4%); Sweden, 63,901 (0.6%); and Switzerland, 26,840 (0.3%). Concussion rates vary by level of participation and diagnostic criteria used with incidences of 1.47 to 1.58 per 1000 athlete exposure (AE) for youth, 0.54 per 1000 AE for high school, 0.5 to 15.8 concussions per 1000 AE)] for Junior A and in NHL, concussions range from 20% to 26% of all injuries (1.45-1.8 concussions [1000 AE]). Helmets reduce head fractures and intracranial bleeds, but their function is influenced by design, material, fit, age, face shields, chin straps, and “J” clips. Mouth guards provide protection against dental injuries, but their role in reducing SRC is not scientifically demonstrated. Concussion severity based on time loss from participation is reduced modestly when full facial protection is worn and players compete on larger ice surfaces. Rule changes favor no-checking leagues and fewer noninjurious head contacts occur with “intensified” compared with “nonintensified” Fair Play rules (16). No significant risk reduction resulted from the NHL’s zero tolerance for head contact rule. Rigorous hockey studies for concussion prevention testing of modifiable intrinsic and extrinsic risk factors, effect modifiers, exposure time, and mechanism of injury are needed (3,17–20).
Psychosocial, psychologic, and psychiatric factors, such as perceived vulnerability, willingness to report, incidence, symptom reports, time loss, playing style, and mental health issues influence SRC rates. Risks associated with sex, sport performance behavior, and mental health have been examined. Injurious hockey behavior increases during games compared with practices and psychiatric factors that influence SRC outcomes. Players with a mental health history and recurrent SRC are at greater risk of depression. SRC clinical risk profiles include anxiety and mood disturbance characterized by hypervigilance, anxiety, and apathy. Psychosocial factors receive little attention in clinical practice literature despite their influence on SRC incidence and recovery. This omission demands further attention (21–25).
Objective 2 — Head Impacts Causing Concussion: A Foundation for Prevention
Head impact biomechanics informed by helmet sensors
The assessment of neurofunctional status after suspected concussion is typically based on subjective symptoms. Player assessments are influenced by awareness and honest reporting. Subjectivity impedes identification of biomechanical thresholds associated with SRC in players consenting to wear accelerometers. Sensors in helmets, patches, and mouthguards report limited information on rads·s2 head movement in SRC.
Head impact sensors monitor head impact exposure (HIE) during practices and games (26,27). These devices record impact frequency, magnitude, and location/direction that enable injury protection strategies and inform helmet design by level of play and sex (27). Players experience HIE at all levels of play, including leagues that do not allow body checking. HIE is sensitive but not specific to SRC diagnosis, confounded by subjective concussion diagnostics (19–22,26,27). HIE enables identification of individual and team at-risk techniques from single and cumulative impacts that trigger medical evaluation, coaching, education, and rule changes. HIE technology assessment and brain injury risk (SRC) has been studied in American football (FB) (23,26,27) but data for hockey is sparse. Injury comparisons between FB and hockey can identify differences in SRC risk and injury mechanism. HIE hockey data has been obtained from Bantam and college players. Comparing Bantam players to same age FB players is more accurate than Bantam to college player comparison. FB players (11-14 years) have reported 252 impacts per player per season (PPS) (28), whereas Bantam and Midget hockey players (13-16 years) had an impact frequency of 223 per PPS (29). Impact severity was greater in youth FB than hockey for mean linear acceleration (25.5g vs. 18.4g) and mean rotational accelerations (1691.8 rad·s−2 vs. 1464.5 rad·s−2). The 95th percentile linear head accelerations experienced by youth FB players (57.3 g) was higher than hockey players (45.6 g), but the rotational accelerations were higher in hockey. Game head impact frequency in same-age FB players occurred at 12.0 impacts per player per game (PPPG) versus 5.2 impacts PPPG among Bantams (13–14 yrs.) (23,25) Data suggest 13- to 14-year-old FB players sustain greater HIE than age matched hockey players, differences that may influence SRC risk. A season of youth FB (13-14 years) was not associated with impaired clinical neurologic function (23,30). This finding might be similar in youth hockey players since they have a lower HIE. There is concern for the young athletes who participate in FB and hockey concurrently, which doubles their SRC risk exposure. Frequent repetitive head impacts separated by short recovery times predispose the brain to injury. Cumulative HIE must always be considered (23,24).
The relationship of head impact events to head accelerations in hockey is known. Falls, collisions, punches, and projectiles cause linear, rotational, and/or angular accelerations that result in quantifiable tissue stress, strain, and strain rates. Magnitude and impact frequency are associated with SRC risk. Increased impact frequency is hypothesized to increase risk of developing CTE. In women’s elite hockey, falls cause 63% of head impacts and 37% of collisions. In men’s elite hockey, collisions account for 80% of head impacts; fights, 8%; and falls, 7%. Video reconstruction of injury events and impact characteristics provide input into finite element modeling (31). Linear accelerations to the head from falls are high, but a punch (uppercut) generates the highest rotational accelerations (rad·s2) and likely results in diffuse axonal injury (DAI). Impact types dictate how energy is transferred to brain tissue (29). The high linear (g) and rotational (rad·s2) accelerations listed in Table must be avoided (28,29,32–35).
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Table: Mean peak linear (g) and rotational (rad·s2) accelerations and maximum principal strain with SD in parentheses for each mechanism of injury.
In summary, reducing HIE at all levels seems practical. Inadvertent head impacts in ice hockey will occur, but purposeful use of the head or involvement of the head during or subsequent to play should be aggressively removed from the sport. HIE can alert coaches and sports medicine providers when worrisome on-ice or locker room events occur.
Video Reconstruction Determines Concussion Causation
Biomechanical analysis of SRC impacts connect head trauma to mechanical responses of brain tissue. SRC detection requires valid measures to assess brain tissue trauma, including impact characteristics: (i) velocity, (ii) compliance, (iii) location, and (iv) impactor mass. Video reconstruction (VR) accurately obtains impact parameters, including direction. VR depicts relationships between (a) linear and rotational accelerations and tissue trauma, (b) the effect of and duration of impact events on tissue trauma, and (c) the relation between brain tissue trauma and SRC risk. Impact frequency and linear acceleration contribute less to understanding SRC in hockey, but provide valuable measures of brain tissue strain, quantification of tissue involved, location and time intervals between events and head trauma duration. These parameters are critical to evaluating sustained trauma and managing subsequent SRC signs and symptoms. Relating dangerous impacts to brain tissue damage, such as SRC, is a valid contribution that video reconstruction provides in our understanding of hockey SRC. This information contributes to the development of SRC prevention strategies (19,28,33,36,37).
Preventing concussion
Concussion prevention tactics include: neck strengthening and anticipation, removal of body checking, behavioral modification (i.e., Fair Play), elimination of fighting and financial incentives in the NHL to discourage dangerous activities.
- (i) Neck strength and anticipation
- Neck strength and concussion awareness may reduce SRC risk and severity (38). Strong neck muscles (39) contracted in collision anticipation can decrease kinematic head response to external forces. A benefit occurs when extension of effective movable mass (the head) moves from neck to torso. Improved neck strength occurs from diverse strengthening programs after short periods. Reduction of SRC risk and severity from stronger neck muscles remains to be proven. Collins followed 6704 men and women in soccer, basketball, and lacrosse. Increased neck strength (measured by hand held dynamometer) decreased concussion odds by 5% (16). Conversely, when Bantams wore HITS helmets, increased cervical neck strength (CNS) did not reduce linear (g) or rotational (rad·s2) accelerations (40). Differences may be explained by subjects, reporting, and measurement methods. Dynamic stiffness, the ability to resist movement from a perturbation force, and hit anticipation were more influential than muscle strength alone (16). Increased stiffness and cervical muscle contraction, when anticipating a “hit,” reduces subsequent head movement. Contraction of the cervical muscles that affix the head to the trunk decreases postimpact head movement/acceleration and reduces SRC risk and severity. Future studies must investigate programs to improve neck strength, muscle performance, and cervical spine dynamic stiffness, in addition to testing the premise “head on a swivel.” These data support penalizing infractions, such as checking from behind, open ice unanticipated and blindside hits that impede players from preemptive neck muscle contraction (6,16,39–44).
- (ii) Body checking
- SRC is reduced by eliminating body checking (BC) in Peewee and ensuring abstinence or optimal checking in Bantams. A three-time greater risk of injury and a four-time greater risk of SRC in Peewee BC leagues compared to non-BC leagues have been reported. BC is a consistent risk factor in youth hockey concussion due to discrepancies in player maturation (height, weight, and skill development). Implementing no BC in Peewee reduced SRC by 67%, a positive finding that must be extended to Bantams.
- (iii) Fair play
- In 1979, Vaz introduced Fair Play (FP) in Quebec to improve hockey safety using behavioral modification (rewards and punishment) to counter both violence and declining participation (45). Teams earn two points for a win, one for a tie, zero for a loss, and a single FPP is awarded for respectful play: available to both winning and losing teams. Excessive penalty minutes by a team (age adjusted), unsportsmanlike behavior by a player, parent, or coach can result in forfeiture of a team’s FPP. Studies looking at injury rates, including concussion, show a decrease in these injuries in tournaments played under FP rules (46). In assessing injury rates, there is evidence suggesting that teams forfeiting their FP point (suggesting a less disciplined style of play) experience a higher injury rate compared with teams that earn their FP point (8,47–50).
- (iv) Fighting
- Although not a major cause of SRC in youth or high school hockey, the complete elimination of fighting in the sport is mandatory. Many players in youth, high school and Junior A aspire to play hockey at higher levels, which motivates them to engage in fighting by taking lessons, practicing in locker rooms, hotels, and sometimes on ice. No fighting should occur at any level because of the immediate and potential long-term consequences, such as CTE (8–10,41,51). A punch to the face has been shown to cause some of the highest recorded rotational accelerations and is clearly a very high-risk mechanism for concussion.
- (v) Can financial concerns and litigation reduce concussion?
- A retrospective cross-sectional study of 323 noncareer-ending concussions in NHL players (2009 to 2012) showed that NHL salary losses of US $42.8 million occurred annually. Payment to retired players over a 20-year period cost the NHL US $135 million. Assumptions that aggressive hockey, including fighting, generates NHL revenue by increasing game attendance, may explain why recommendations to reduce head trauma in professional hockey have been ignored. Such arguments might be countered by (i) salary expenses from absent and retired SRC players, (ii) medical costs to treat head injuries, (iii) lost ticket sales and television revenue when star players are sidelined, (iv) criticism of the NHL when their SRC stance is publicized, and (v) the financial toll of SRC on the NHL is significant (9,43).
Objective 3 — Diagnosing Concussion: What Tests Are Reliable and Evolving?
It is imperative that the pathophysiology of concussion is understood prior to diagnosing. SRC pathophysiology relates to clinical findings, injury response, and recovery time. SRC is manifested by (a) ionic flux and neurotransmitter release, (b) neurometabolic cascade and energy crisis, (c) axonal dysfunction and injury, (d) synaptic dysfunction, (e) blood brain barrier and cerebral blood flow (CBF) changes, (f) glial reactivity and neuroinflammation, (g) impaired glymphatic clearance, (h) altered protein homeostasis, and (i) potential neurodegeneration (10,51). Post-SRC dysfunction may manifest as migraine symptoms, impaired cognition and processing, lack of coordination, behavioral changes, CBF changes, slowed learning and plasticity. Imaging postacute mTBI shows (CBF) alterations may outlast symptoms and neurocognitive impairment (NCI). SRC neurobiological response progresses from seconds to minutes with full recovery requiring weeks or perhaps longer. Studies are clarifying links between acute SRC pathophysiology progression to chronicity and neurodegeneration (CTE, Parkinson’s disease, and Alzheimer’s disease). The Mayo Clinic Ice Hockey Research team developed an evolving Objective Diagnosis of Concussion. Although the data are collected at rink side, it is not yet used in initial diagnoses. As such, clinical diagnoses at rink side and medical diagnoses made in the clinic are appropriately discussed first (10,51–54).
Diagnosing Concussion in Players at Rink Side
Ideally, a hockey knowledgeable, trained medical professional (athletic trainer, physician, and physical therapist) is present to assess players suspected of SRC and reduce risks of returning concussed players to play. Experienced providers astutely observe mechanism of head impacts and subsequent player behavior. Baseline testing preseason provides comparisons for subsequent assessments, including a symptom scale, cognitive, and balance tests (Sideline Assessment of Concussion Test [SCAT5]) and rapid number naming tests (King-Devick Test). Players are removed from the game or practice if findings are consistent with SRC: observed mechanism of injury, signs, symptoms, abnormal physical examination, cognitive, balance, or oculomotor tests as compared with baseline (51,52,54–56).
Diagnosing Concussions and Determining Severity in a Medical Setting
Despite promising biomarkers, an SRC clinical diagnosis requires a focused and relevant history and examination. Of importance is timing, mechanism, head impact location of current SRC, symptoms and signs including loss of consciousness, amnesia, risk factors, post-SRC sequelae, and a history of previous concussions and the duration of symptoms. If a prior history of concussion exists, lower SRC acceleration thresholds (lesser magnitude of impact) will result in concussion. Only 50% have symptom severity scores (SSS) of zero at baseline, supporting mandatory baseline assessment. Firm recommendations on which specific baseline tests will require validation for different groups, proper testing conditions, and use of appropriate normative data and consideration of practice effects are needed. Currently, documented meaningful change is six points on the SSS. SCAT-5 contains a useful cognition test (sensitivity 64% to 89% and specificity 76% to 91%). The Montreal Cognitive Assessment and computerized NP assessments (i.e., Cogstate or ImPACT) can supplement the Sideline Assessment of Concussion (SAC). Portions of the neurologic examination are core to SRC office evaluations. Assessing dynamic balance and vestibular function (e.g., timed tandem gait), oculomotor function (King-Devick Test, convergence insufficiency), and vestibuloocular reflex (dynamic visual acuity, head impulse test) are essential elements in the office examination of a SRC. Food and Drug Administration-approved devices to assess balance now include Sway balance and a King-Devick balance test app (14,56–62).
Motor Impairments and Musculoskeletal Injury Risk after Return to Play
Accumulating evidence suggests post-SRC athletes have subclinical deficits in neurocognition and neuromuscular control after a concussion, resulting in an increased risk of subsequent lower extremity injury after return to play (RTP). Additional studies of cognitive and motor performance during dual-task conditions showed that concussed athletes demonstrate ongoing impairments in gait and balance even when performance on standard clinical measures had recovered (63). RTP assessment of concussed athletes must include clinical tests of neuromuscular responsiveness under challenging sport-like conditions (57,63,64).
Importance of Objective Diagnoses of Concussion
Objective components of an SRC diagnosis (King-Devick Test, QEEG, and promising fluid neurobiomarkers shown in Fig. 1) are aligning in research with SRC signs and symptoms. These tests need further validation before they can be relied on for diagnosis or to guide management of hockey SRC. The Berlin Consensus (or work by McCrae) identified similar components of promising measures emerging for clinical diagnoses and to guide and ultimately evaluate treatment effect (14,19,62,65,66). Valid, objective diagnostic tests are needed to reduce either unreported (denied) or the opposite (exaggerated) symptoms and signs of SRC. Adding criteria to help determine diagnostic clinical certainty of concussion — definite, probable, possible — has been proposed.
Figure 1: Although no figure of the Objective Diagnosis of Concussion Components was published previously the components were described in a publication (
19). These three components include the NeuroCatch (QEEG), the King-Devick Test, and a photo of phlebotomy test tubes used in the testing of serum neurobiomarkers.
Using the King-Devick Test in Concussion Diagnosis
Eye movement and vision-related tasks involve 55% of brain pathways integral to brain integrity and are vulnerable in SRC. Rink-side SRC evaluation includes oculomotor assessment that contributes valid, critical, and objective data with greater accuracy and speed than balance and cognitive tests alone. Many SRC are not witnessed and more than 50% of athletes do not report SRC symptoms. The King-Devick Test (KDT) is a fast, valid, reliable, rapid number naming test that objectively identifies post-SRC suboptimal brain function. A meta-analysis of KDT data showed 86% sensitivity and 90% specificity for SRC, with five times greater risk of SRC (relative risk = 4.92) if KDT time and accuracy worsens between baseline and SRC testing. KDT successfully distinguished between concussed versus control in youth and collegiate athletes (receiver operating characteristic: KDT 0.92; timed tandem gait 0.87; SAC 0.68). A 3-year study of rugby players demonstrated six times more unwitnessed/unreported concussions than witnessed SRC. All were identified with KDT (100% sensitivity, 94% specificity) including players with no clinical signs or symptoms. KDT is reliably administered by medical professionals as well as trained nonmedical individuals, such as coaches and parents (62,67–70).
Quantified EEG (QEEG)
The objective evaluation of brain vital signs is possible with portable electroencephalography (EEG). Derived from established event-related potentials (ERPs) (i.e., N100, P300, and N400) provide a fast and automated evaluation of brain wave responses normatively quantified. Brain function changes in 47 Junior A hockey players post-SRC were evaluated using a repeated measure design (baseline, post-SRC, RTP, and postseason). SRC was hypothesized to cause significant changes in response amplitude and latency, proving that brain vital signs are significantly changed after a SRC. Differences between baseline and RTP indicated persistent impairment despite a lack of clinical detection. Interestingly, significant subconcussive changes in brain vital signs for preseason and postseason testing of players who did not sustain SRC further suggest enhanced sensitivity to concussion-related effects on brain function. Radar plots (Fig. 2) showed systematic changes across six brain vital signs scores depicted by a unique “profile” when baseline hexagonal shape transforms into a triangular shape, due to consistent increases in amplitude and decreases in latency for SRC. Support is evolving for the use of brain vital signs as an objective, physiological measurement of SRC (24,71,72).
Figure 2: This figure of radar plots shows systematic changes across brain vital sign scores. The profile shows the hexagonal shape evolving into a triangular shape influenced by the increased amplitude and decreased latency that occurs postconcussion.
Fluid Biomarkers
Identifying objective biomarkers from neuronal, axonal and astroglial injury may aid SRC diagnosis (19), assess severity and predict prognosis. In addition, biomarkers in blood (61) or saliva may help determine potential long-term consequences of repetitive subconcussive blows, recurrent SRC, and progressive neurodegenerative disease. Objective neurobiomarker results post-SRC will support medical personnel counseling at-risk SRC individuals. McCrea and colleagues reviewed the role of biomarkers in assessing SRC (14). Eleven of 16 studies (14 blood +2 saliva) showed that biomarkers aid SRC diagnosis (AMPAR, S100B, T-Tau, marinoburagenin, PSCPP, GFAP, NSE, SNTF, tau-C, metabolomics profiling). Although four showed evidence in predicting outcomes (SNTF, quinolinic acid, prolactin, tau-A), the level of evidence for fluid biomarker utility in clinical assessment of SRC was rated as low. MicroRNA, comprised of short, noncoding nucleic acids that regulate protein expression, travel through extracellular fluid in exosomes and are detectable in saliva. MicroRNA is functionally related to genes in the brain and values are altered after SRC, reflecting symptom character and duration. Blood and salivary biomarkers may play a role in SRC diagnosis, severity, prognosis, and RTP decision making. They are important research tools requiring further validation before they can be relied on for a SRC diagnosis or severity prediction (14,19,61).
Metabolomic Profiling
Significant acute symptoms may linger after an SRC, manifested by chronic long-term neurologic dysfunction (Post-Concussion Syndrome). Concussion diagnosis and RTP decision making are difficult. Plasma metabolomic profiling as a diagnostic tool indicates SRC in youth hockey players can be accurately diagnosed (>90% diagnostic accuracy; P < 0.0001). SRC causes a specific metabolomic pattern characterized by decreased plasma glycerophospholipids. Metabolomics data were supported by MRI showing diffusion abnormalities within multiple white matter tracts, functional hyper connectivity, and decreases in choline 3 months after concussion. Metabolomic profiling, together with multivariate statistical analysis and machine learning, represents a novel diagnostic method for SRC that may be amenable to future point-of-care testing. These diagnostic tests are not yet ready for clinical application, but show promise for prompt SRC identification and severity prediction (11,73).
Contributing Consultations - Use of Neuroimaging
Computed tomography (CT) is the preferred imaging modality for moderate and severe neurotrauma to detect hemorrhagic intracranial lesions including intraparenchymal hematomas, subdural and epidural hematomas, subarachnoid hemorrhage, in addition to facial and skull fractures. However, diffuse axonal injury and petechial hemorrhages resulting from a concussion are not apparent on CT. Advanced MRI techniques characterize traumatic brain injuries in these CT negative lesions. Studies show reduced brain volume, even in subjects with normal T2 imaging. Focal reduced volume of the left cingulate negatively correlates with post-SRC anxiety and other symptoms. Diffusion imaging (DI) has been shown to demonstrate lower fractional anisotropy (FA) with more significant changes in the temporal and occipital lobes. These FA changes are associated with significantly poor memory scores. Diffusion tractography demonstrates reduced tract size and focal disruption in fiber bundles. Functional MR demonstrates network activity disruption following mTBI. Also, increased functional activity has been shown post-SRC. This increased activity reflects that higher levels of brain activity are required to perform memory tasks competently as well as normal controls. MR spectroscopy provides a quantitative measure of brain injury and can identify functional abnormalities in normal-appearing athletes post-mTBI. N-acetylaspartate (NAA), a measure of neuronal health, decreases in SRC. NAA to creatine ratios have been proposed as a method to acutely assess severity of brain injury and follow recovery. Brain biomarkers detectable with advanced MRI techniques are helpful to understand the impact of SRC. Future research must focus on metrics to evaluate individual athletes post-SRC in acute care settings. Accurate imaging techniques to detect mTBI and subsequently to confirm recovery are important steps forward in the care of SRC (12,74–76).
Session 5 – Expert Panel Ideas for Action on Concussion
Panels
Nine experts, including health care professionals, former NHL hockey players, and USA Hockey’s coaching, officiating and safety leaders shared their hockey concussion experiences. These panelists bridged the gap between sophisticated medical knowledge and the harsh realities of competitive hockey. For example, an NHL player was asked if he openly admitted to his concussion symptoms and he replied “What, are you kidding, and lose my job?”
Objective 4 - Taking Science and Treatment Forward: From Bench to Clinic and Rink Side
In vitro models for brain injury
In vitro experimental models capable of finely controlling forces and deformations exerted on cells must be developed in order to understand mechanical force effect on neuronal health and function when head injury (SRC) occurs. Methods proposed include: physical impact, fluid percussion, fluid shear stress, and high-speed stretching models. These models consistently show mechanical injury leads to focal swelling, indicative of diffuse axonal injury. However, connections between head injury trauma and lasting dysfunctional chronic traumatic encephalopathy (CTE) are not known. Neurofibrillary tangles accumulating where large stresses are expected post head injury, suggest a direct connection between cell trauma and CTE development. In vitro models of mechanically induced dysfunction, combined with computational modeling of brain deformation during head injury could provide important insights into concussion pathways and potential treatment to prevent CTE in concussed hockey players (77–81).
Using Hockey Accelerations to Examine an Animal Behavioral Model
Injury risk curves relate neurofunctional status following exposure to biomechanical events (i.e., applied forces or head movement). Animal laboratory models can test SRC risk relationships to rapid head rotation, magnitude, and direction and to influences of age, sex, and previous SRC on biomechanical SRC thresholds. TBI animal models exhibit LOC, axonal damage, hemorrhage, and focal contusions in contrast to the subtle, subjective, cognitive, neurofunctional alterations found in players with SRC. Animal models provide insight into how head impacts and sudden head movements produce brain deformations that cause brain injuries (mTBI to TBI). Emerging research in objective, involuntary neurofunctional metrics and biomarkers are bridging gaps between human and animal research. SRC biomechanics provide a rational research foundation to test hockey SRC prevention strategies (82–86).
Pharmacologic Interventions Available Now and on the Horizon
Concussion is a complex multiphasic brain injury initially caused by a blunt force, followed by secondary injury involving meningeal and parenchymal inflammation, generation of reactive oxygen species, glutamate excitotoxicity, blood brain barrier (BBB) permeability, microglial activation, neutrophil infiltration, cellular edema, axonal injury, microtubule disassembly, and apoptosis. Biochemical and molecular factors involved in these injury cascades are targets for acute therapy to minimize/prevent secondary injury and mitigate neurological sequelae. Therapy to decrease inflammation and minimize secondary cascades are not available, thus research on treatment should be an SRC priority for investigators.
The secondary cascade (inflammatory oxidative crisis) causing cell death can be reduced by glutathione in concussion animal models. Preclinical evidence suggests the calcitonin gene-related peptide (CGRP) pathway may be a new target for drugs and monoclonal antibodies, especially for postconcussion headache. Preclinical and preliminary human evidence of efficacy for N-acetyl-cysteine (NAC) has been demonstrated to reduce postconcussion symptoms in a controlled study of military operators who sustained a blast injury-related concussion. In 2016, a study of thioredoxin-mimetic peptides (TXM peptides) reported protection of cognitive function post-mTBI in mice (87). Astaxanthin also improved cognitive performance post-mTBI in animals; this dietary carotenoid protects via anti-inflammatory and antioxidants (87–92).
Fish Oils, Supplements, and their Neuroprotective Effects
SRC induced by any forces to the brain may lead to symptoms and/or signs with or without loss of consciousness (LOC). SRC is predominantly functional despite the fact that neuropathological changes occur. SRC increases metabolic demand, impairs metabolism, decreases CBF, and results in hypometabolism with symptoms persisting from 1 to 4 wk. Nutritional supplements are hypothesized to provide neuroprotective/therapeutic effects. Ecosapentaneoic acid (EPA) and docosahexaenoic acid (DHEA) are omega-3 fatty acids found in human neuronal and synaptic vesicle plasma membranes involved in inter- and intracellular signaling. These fatty acids influence apoptotic death via gene expression modulation. Several animal studies demonstrate post-mTBI protective effects of DHEA and EPA alone or in combination. Animal model studies demonstrate recovery following TBI with DHEA and EPA supplementation. Other supplements with strong anti-inflammatory (curcumin) or antioxidant properties, such as reservatrol, melatonin, and S. Baicalensis also show improved postconcussion recovery in animal models. Creatine, vitamin C, and vitamin E improve TBI outcomes in humans, but have not been evaluated in SRC. Vitamin D enhances TBI outcomes in animal and human studies when combined with progesterone, a combination not yet studied in SRC. Preliminary animal and severe TBI human studies are promising; however, current evidence does not prove that nutritional supplements prevent or effectively treat SRC (53,93–97).
Postconcussion Syndrome (PCS)
The Fifth International Conference on Concussion in Sport (2016) defined PCS as an mTBI with symptoms persisting >14 d for adults and >4 wk for children. PCS contributors include symptom severity, previous concussion, migraine, psychiatric history, adolescence, and female sex. Symptoms include headache, fatigue, noise or light sensitivity, dizziness, imbalance, disturbed sleep, irritability, emotional lability, anxiety, depression and inattention, concentration, memory, and thinking quickly. Structural brain and cervical injuries, chronic headaches, pain, vestibular and/or sleep disorders, depression, anxiety, adjustment disorders, ADHD, medication side effects, or drug and/or alcohol abuse must be excluded. PCS evaluation requires a comprehensive history of injury mechanism, initial and current symptoms, interval treatment, and medical and concussion history. The examination should address the vestibular, oculomotor, cervical spine, and neurologic systems. Neuropsychological (NP) testing identifies cognitive, behavioral, and affective deficit severity to establish a baseline to track recovery. Aerobic exercise without symptom exacerbation is recommended. PCS patients may have reduced exercise capacity with shorter duration, higher perceived exertion and lower heart rate. Neuroimaging (fMRI, DTI, MRS), blood biomarkers, genetic testing, and QEEG are promising adjuncts to evaluation. Current PCS management requires medical, physical, and psychosocial assessment using a multidisciplinary, patient-centered approach. Educational materials (verbal and written), school accommodations, physical rehabilitation (symptom limited, personalized aerobic exercises, targeted vestibular, visual, proprioception and musculoskeletal (cervical spine) therapeutic exercise, and psychological consultation (reassurance, anxiety/stress management and cognitive behavioral therapy need to be addressed. Cognitive rehabilitation emphasizes compensatory training, “brain breaks,” and coping strategies. Nonpharmacological methods initially treat headache, sleep, and mood disorders. Medications with sedating side effects must be avoided, whereas education and reassurance are central to concussion management and the player’s gradual return to activity (1).
Session 7 — Evolving Scientific Contributions
Effective exercise regimens for postconcussion benefit
SRC adversely affects the autonomic nervous system (ANS) and CBF control. Guided aerobic exercise benefits blood pressure, CBF control and CO2 sensitivity in post-SRC-persistent postconcussive symptoms (PPCS). Although evidence-based treatment is on the horizon for acute SRC, consensus-based recommendations emphasize rest until asymptomatic. New evidence suggests excess rest prolongs recovery, whereas moderate physical activity (PA) 1-wk post-SRC may reduce post-SRC-PPCS incidence. A systematic evaluation of exercise tolerance (Buffalo Concussion Treadmill Test) in players with PPCS followed by prescription of a controlled, subthreshold exercise regimen showed a safe, speedy recovery. Preliminary data show subthreshold exercise may speed recovery if administered the first week post-SRC. This finding challenges the recent world consensus recommendation that athletes rest post-SRC until symptoms stabilize. Athletes should be active but remain below cognitive and physical symptom-exacerbation thresholds. Strict abstinence of activity beyond a few days postconcussion is likely detrimental to SRC recovery. Moderate activity and aerobic exercise below symptom exacerbation appear safe and may speed recovery and potentially prevent post-SRC players from developing PPCS. Medication, supplements, and exercise are promising, but preventing initial and recurrent SRC is most important (54,98–101).
Concussion Awareness: Positive or Negative for Concussion?
Concussion awareness has increased in sports including hockey, yet its effect across hockey participation age groups is not known. Although youth sport registration has increased across decades, some sports have recently experienced attrition. Participation variation may be attributed to economic issues, increased specialization, and SRC. Participation in youth and high school FB along with sports with similar SRC risk has decreased. The national increase in hockey participation may be attributed to better education for hockey stakeholders, including athletes, parents, coaches, and medical providers. Despite a decade of youth hockey growth, 2011 to 2013 registration rates dropped locally and nationally. A potential explanation may have been the NHL lock-out and concurrent reports of concussion and neurologic injuries. Hockey participation rates continue to increase and may be influenced by concussion education, rule changes, and behavioral modification (102–105).
Opportunities and Barriers to Eliminate Fighting from Hockey
Fighting in hockey is learned and sustained by role modeling. NHL and Junior A hockey leagues tolerate fighting despite the fact that fans studied across 13 years favored skilled play and “no fighting.” The act of fighting causes repetitive head impacts and traumatic brain accelerations that contribute to SRC. Concern about the frequency and consequences of SRC provides opportunities to eliminate fighting and reduce head hits at all levels of play. Currently, proud Junior A players track their fights on www.hockeyfights.com. Repeated head trauma effects, including suicides in players whose role is to fight, should be viewed through the lens of the neurometabolic cascade. Head hits in hockey create an oxidative crisis, diffuse axonal injury, and may contribute to the development of CTE. All head trauma is harmful, but a punch delivered at an angle and a fall to the ice without a helmet result in some of the highest rotational accelerations. Zero tolerance for all head trauma requires rigorous rule enforcement and a fundamental change in hockey. Reducing head trauma requires the elimination of fighting, checking from behind, boarding, elbowing, and locker room boxing. A designated individual on each team (Coach or “Safety Parent”) should supervise player locker rooms at every home and away game. Annual preseason Safety Clinics can reinforce these messages. Fair Play expansion, elimination of body checking at the Bantam level, and automatic game ejection for fighting were prioritized at the Ice Hockey Summit III (2017). Neurolaw will help apply scientific advancement to improved concussion policy (19,37,51,77,106).
The International Ice Hockey Federation, International Olympic Committee, Federation Internationale de Football Association, World Rugby Association, and Federation Equestre Internationale hosted 30 concussion experts and 410 participants in 2016 for a 2-d conference. The experts developed guidelines from a systematic literature review, meeting discussions, and consensus building. Emphasis was placed on concussion education, detection, and prevention (107).
The Role of Science in Society: Research, Education, and Practice
State concussion laws help translate emerging scientific knowledge into SRC policy. Following Washington’s lead in 2009, 50 states have enacted a youth SRC law. Each research community must partner with stakeholders to ensure accountability. A policy challenge is facilitating accurate communication of risks and benefits to inform athlete and parent decisions. Accomplishing that objective mandates stakeholders to understand SRC statutes and think creatively about next steps. All stakeholders must work as a team and strive to improve youth SRC policy, guided by five foundational principles: collaborative, feasible, scientifically sound, fidelity of implementation, and alignment of incentives. Evaluation requires the alignment of incentives of schools and youth leagues to maintain high levels of participation. Challenges pertain to “fidelity of implementation,” which assesses how stated policy is executed in practice. What is written is often not followed. For instance, in an ongoing NHL litigation, medical staff clearly diverge from SRC protocols in some pressured situations. Variation is expected in youth hockey, and research is designed accordingly. There also is a potential for regional, socioeconomic, and racial variation in implementation of SRC hockey policy (108).
Three panels interspersed during the Summit contributed significantly to the curriculum: panel A comprised of three former NHL hockey players with a history of significant concussion who discussed solutions. Panel B engaged three medical providers with hockey concussion expertise to obtain their ideas to address the concussion epidemic. Panel C benefited from the experience of USA Hockey Directors of Officiating, Coaching Education, and Player Safety.
Objective 5 — Integrating Science and Clinical Care into Our Action Plan
Session 9 — Concluding Ice Hockey Summit III
Strategic action items designed to reduce the risk and severity of SRC from each academic session were projected and voted on for prioritization by all Summit attendees (3) (Fig. 3).
Figure 3: Listed are the action items voted on most highly for the five content categories at the Summit. The categories were: 1) Epidemiology, Etiology, and Risk of Concussion, 2) Prevention of Concussion, 3) Subjective and Objective Diagnostic Tests and Future Directions, 4) Treatment Method to Enhance Recovery Now and in the Future, and 5) Integrating Science and Concussion Care into Policy.
Drs. Stuart and Smith express their appreciation to Pam Otterbein, Sierra Tollefson, and Linda Gochnauer for their preparation for and execution of the Summit III. Thank you to Kevin Koenings who obtained seamless audiovisual presentations for speakers presenting in person and for those presenting from elsewhere. Drs. Chip Burke, Michael Joyner, William Roberts, Chad Eickhoff, ATC, MSc, and Shaun Fickling, PhD (candidate), are thanked for their medical and scientific advice. Drs. Nicole LaVoi and James Whitehead capably presented on social media and initiating takeaway messaging. Shjon Podein gave a thoughtful and memorable personal account of his professional hockey career. We appreciated panelists (previously NHL players) Mike Eaves, Michael B. Stuart, MD, and Jordan Leopold, and panelists from USA Hockey Matt Leaf, Mark Trabrum, and Kevin Margarucci. Thank you to Matthew Hanzel, J.D., for his valuable contributions. Thank you to our supporting organizations: USA Hockey, International Ice Hockey Federation (IIHF), Thorne Science, Hockey Equipment Certification Committee (HECC), American College of Sports Medicine (ACSM), Johannson-Gund Endowment, Brian Mark Foundation, and our Martineau Gift.
References
1. McCrory P, Meeuwisse W, Dvořák J, et al. Consensus statement on concussion in sport—the 5th International Conference on Concussion in Sport held in Berlin, October 2016.
Br. J. Sports Med. 2017; 51:838–47.
2. Kontos AP, Elbin RJ, Sufrinko A, et al. Incidence of concussion in youth ice hockey players.
Pediatrics. 2016; 137:e20151633.
3. Smith AM, Stuart MJ, Dodick DW, et al. Ice Hockey Summit II: zero tolerance for head hits and fighting.
Curr. Sports Med. Reports. 2015; 14:135–44.
4. Smith AM, Stuart MJ, Greenwald RM, et al. Proceedings from the Ice Hockey Summit on Concussion: a call to action.
Clin. J. Sport Med. 2011; 21:281–7.
5. Benson BW, Meeuwisse WH. Ice hockey injuries. In: Maffoli N, Caine DJ, editors.
Epidemiology of Pediatric Sports Injuries. Karger Publishers; 2005; p. 86–119.
6. Black AM, Hagel BE, Palacios-Derflingher L, et al. The risk of injury associated with body checking among Pee Wee ice hockey players: an evaluation of Hockey Canada’s national body checking policy change.
Br. J. Sports Med. 2017; 51:1767–72.
7. Marar M, McIlvain NM, Fields SK, Comstock RD. Epidemiology of concussions among United States high school athletes in 20 sports.
Am. J. Sports Med. 2012; 40:747–55.
8. Donaldson L, Li B, Cusimano MD. Economic burden of time lost due to injury in NHL hockey players.
Inj. Prev. 2014; 20:347–9.
9. Hiploylee C, Wennberg R, Tator CH. The financial toll of career-ending concussions in professional hockey.
Concussion. 2016; 1:CNC20.
10. Barkhoudarian G, Hovda DA, Giza CC. The molecular pathophysiology of concussive brain injury–an update.
Phys. Med. Rehabil. Clin. N. Am. 2016; 27:373–93.
11. Manning KY, Schranz A, Bartha R, et al. Multiparametric MRI changes persist beyond recovery in concussed adolescent hockey players.
Neurology. 2017; 89:2157–66.
12. Slobounov SM, Zhang K, Pennell D, et al. Functional abnormalities in normally appearing athletes following mild traumatic brain injury: a functional MRI study.
Exp. Brain Res. 2010; 202:341–54.
13. Patricios JS, Ardern CL, Hislop MD, et al. Implementation of the 2017 Berlin Concussion in Sport Group Consensus statement in contact and collision sports: a joint position statement from 11 national and international sports organisations.
Br. J. Sports Med. 2018; 52:635–41.
14. McCrea M, Meier T, Huber D, et al. Role of advanced neuroimaging, fluid biomarkers and genetic testing in the assessment of sport-related concussion: a systematic review.
Br. J. Sports Med. 2017; bjsports-2016-097447.
15. Wiese-Bjornstal DM, White AC, Russell HC, Smith AM. Psychology of sport concussions.
Kinesiol Rev. 2015; 4:169–89.
16. Schmidt JD, Pierce AF, Guskiewicz KM, et al. Safe-play knowledge, aggression, and head-impact biomechanics in adolescent ice hockey players.
J. Athl. Train. 2016; 51:366–72.
17. Smith A, Stuart M, Greenwald R, et al. Proceedings from the ice hockey summit on concussion: a call to action.
Clin. Neuropsychol. 2011; 25:689–701.
18. Smith AM, Gaz DV, Larson D, et al. Does fair play reduce concussions? A prospective, comparative analysis of competitive youth hockey tournaments.
BMJ Open Sport Exerc. Med. 2016; 2:e000074.
19. Smith AM, Stuart MJ, Roberts WO, et al. Concussion in ice hockey: current gaps and future directions in an objective diagnosis.
Clin. J. Sport Med. 2017; 27:503–9.
20. Brainard LL. Gender differences in head impacts sustained by collegiate ice hockey players.
Med. Sci. Sports Exerc. 2012; 45:747–54.
21. Wilcox B. Biomechanics of head impacts associated with diagnosed concussion in female collegiate ice hockey players.
J. Biomech. 2015; 48:2201–4.
22. Wilcox BJ, Beckwith JG, Greenwald RM, Crisco JJ. Limitations of “validation study of helmet-based impact measurement system in hockey”.
Med. Sci. Sports Exerc. 2014; 46:640.
23. Munce TA, Dorman JC, Thompson PA, et al. Head impact exposure and neurologic function of youth football players.
Med. Sci. Sports Exerc. 2015; 47:1567–76.
24. Mihalik JP, Guskiewicz KM, Marshall SW, et al. Head impact biomechanics in youth hockey: comparisons across playing position, event types, and impact locations.
Ann. Biomed. Eng. 2012; 40:141–9.
25. Reed N, Taha T, Keightley M, et al. Measurement of head impacts in youth ice hockey players.
Int. J. Sports Med. 2010; 31:826–33.
26. Beckwith JG, Greenwald RM, Chu JJ, et al. Head impact exposure sustained by football players on days of diagnosed concussion.
Med. Sci. Sports Exerc. 2013; 45:737.
27. Beckwith JG, Greenwald RM, Chu JJ, et al. Timing of concussion diagnosis is related to head impact exposure prior to injury.
Med. Sci. Sports Exerc. 2013; 45:747.
28. Kendall M. Comparison and characterizatoin of different concussive brain injury events [dissertation].
Universite d’Ottawa/University of Ottawa. 2016. 190 p.
29. Oeur RA, Gilchrist MD, Hoshizaki TB. Interaction of impact parameters for simulated falls in sport using three different sized Hybrid III headforms.
Int. J. Crashworthiness. 2018; 1–10.
30. Munce TA, Dorman JC, Odney TO, et al. Effects of youth football on selected clinical measures of neurologic function: a pilot study.
J. Child Neurol. 2014; 29:1601–7.
31. Hoshizaki TB, Post A, Oeur RA, Brien SE. Current and future concepts in helmet and sports injury prevention.
Neurosurgery. 2014; 75(Suppl 4):S136–48.
32. Hutchison MG, Comper P, Meeuwisse WH, Echemendia RJ. A systematic video analysis of National Hockey League (NHL) concussions, part I: who, when, where and what?
Br. J. Sports Med. 2015; 49:547–51.
33. Post A, Oeur A, Hoshizaki B, Gilchrist MD. Examination of the relationship between peak linear and angular accelerations to brain deformation metrics in hockey helmet impacts.
Comput. Methods Biomech. Biomed. Engin. 2013; 16:511–9.
34. Oeur RA, Karton C, Post A, et al. A comparison of head dynamic response and brain tissue stress and strain using accident reconstructions for concussion, concussion with persistent postconcussive symptoms, and subdural hematoma.
J. Neurosurg. 2015; 123:415–22.
35. Zhang L, Yang KH, Dwarampudi R, et al. Recent advances in brain injury research: a new human head model development and validation.
Stapp Car Crash J. 2001; 45:369–94.
36. Sano K, Nakamura N, Hirakawa K, et al. Correlative studies of dynamics and pathology in whip-lash and head injuries.
Scand. J. Rehabil. Med. 1972; 4:47–54.
37. Hoshizaki B, Post A, Kendall M, et al. The relationship between head impact characteristics and brain trauma.
J. Neurol. Neurophysiol. 2013; 5:1–8.
38. Mihalik JP, Guskiewicz KM, Marshall SW, et al. Does cervical muscle strength in youth ice hockey players affect head impact biomechanics?
Clin. J. Sport Med. 2011; 21:416–21.
39. Eckner JT, Oh YK, Joshi MS, et al. Effect of neck muscle strength and anticipatory cervical muscle activation on the kinematic response of the head to impulsive loads.
Am. J. Sports Med. 2014; 42:566–76.
40. Mansell J, Tierney RT, Sitler MR, et al. Resistance training and head-neck segment dynamic stabilization in male and female collegiate soccer players.
J. Athl. Train. 2005; 40:310–9.
41. Black A, Palacios-Derflingher L, Schneider KJ, et al. The effect of a national body checking policy change on concussion risk in youth ice hockey players.
Br. J. Sports Med. 2017; 51:A70–1.
42. Emery CA, Kang J, Schneider KJ, Meeuwisse WH. Risk of injury and concussion associated with team performance and penalty minutes in competitive youth ice hockey.
Br. J. Sports Med. 2011; 45:1289–93.
43. Benson BW, Meeuwisse WH, Rizos J, et al. A prospective study of concussions among National Hockey League players during regular season games: the NHL-NHLPA Concussion Program.
Can. Med. Assoc. J. 2011; 183:905–11.
44. Emery C, Kang J, Shrier I, et al. Risk of injury associated with bodychecking experience among youth hockey players.
Can. Med. Assoc. J. 2011; 183:1249–56.
45. Emery CA, Kang J, Shrier I, et al. Risk of injury associated with body checking among youth ice hockey players.
JAMA. 2010; 303:2265–72.
46. Emery CA, Black AM, Kolstad A, et al. What strategies can be used to effectively reduce the risk of concussion in sport? A systematic review.
Br. J. Sports Med. 2017; 51:978–84.
47. Vaz EW, Clarke W.
The Professionalization of Young Hockey Players. Lincoln (NE): University of Nebraska Press. 1982.
48. Roberts WO, Brust JD, Leonard B, Hebert BJ. Fair-play rules and injury reduction in ice hockey.
Arch. Pediatr. Adolesc. Med. 1996; 150:140–5.
49. Smith AM, Jorgenson M, Sorenson MC, et al. Hockey Education Program (HEP): a statewide measure of fair play, skill development, and coaching excellence.
J. ASTM Inter. 2009; 6:1–14.
50. Smith AM, Stuart MJ, Colbenson CM, Kronebusch SP.
A Psychosocial Perspective of Aggression in Ice Hockey. In: Ashare AB, editor. Safety in Ice Hockey. 3rd vol. West Conshohocken (PA): ASTM International; 2000.
51. Giza CC, Hovda DA. The new neurometabolic cascade of concussion.
Neurosurgery. 2014; 75(Suppl 4):S24–33.
52. Meier TB, Bellgowan PS, Singh R, et al. Recovery of cerebral blood flow following sports-related concussion.
JAMA Neurol. 2015; 72:530–8.
53. Giza CC, Hovda DA. The neurometabolic cascade of concussion.
J. Athl. Train. 2001; 36:228–35.
54. Clausen M, Pendergast DR, Willer B, Leddy J. Cerebral blood flow during treadmill exercise is a marker of physiological postconcussion syndrome in female athletes.
J. Head Trauma Rehabil. 2016; 31:215–24.
55. Wilcox BJ, Machan JT, Beckwith JG, et al. Head-impact mechanisms in men’s and women’s collegiate ice hockey.
J. Athl. Train. 2014; 49:514–20.
56. Galetta KM, Brandes LE, Maki K, et al. The King–Devick test and sports-related concussion: study of a rapid visual screening tool in a collegiate cohort.
J. Neurol. Sci. 2011; 309:34–9.
57. Howell DR, Osternig LR, Chou L-S. Single-task and dual-task tandem gait test performance after concussion.
J. Sci. Med. Sport. 2017; 20:622–6.
58. Maruff P, Thomas E, Cysique L, et al. Validity of the CogState brief battery: relationship to standardized tests and sensitivity to cognitive impairment in mild traumatic brain injury, schizophrenia, and AIDS dementia complex.
Arch. Clin. Neuropsychol. 2009; 24:165–78.
59. Echemendia RJ, Meeuwisse W, McCrory P, et al. The sport concussion assessment tool 5th ed. (SCAT5): background and rationale.
Br. J. Sports Med. 2017; 51:848–50.
60. Nasreddine ZS, Phillips NA, Bedirian V, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment.
J. Am. Geriatr. Soc. 2005; 53.
61. Zetterberg H, Smith DH, Blennow K. Biomarkers of mild traumatic brain injury in cerebrospinal fluid and blood.
Nat. Rev. Neurol. 2013; 9:201.
62. Galetta KM, Morganroth J, Moehringer N, et al. Adding vision to concussion testing: a prospective study of sideline testing in youth and collegiate athletes.
J. Neuroophthalmol. 2015; 35:235–41.
63. Howell DR, Lynall RC, Buckley TA, Herman DC. Neuromuscular control deficits and the risk of subsequent injury after a concussion: a scoping review.
Sports Med. 2018; 48:1097–115.
64. Howell DR, Stillman A, Buckley TA, et al. The utility of instrumented dual-task gait and tablet-based neurocognitive measurements after concussion.
J. Sci. Med. Sport. 2018; 21:358–62.
65. Jorgensen JK, Thoreson AR, Stuart MB, et al. Interpreting oblique impact data from an accelerometer-instrumented ice hockey helmet. Proceedings of the Institution of Mechanical Engineers, part P.
J. Sport Eng. Technol. 2017; 231:307–16.
66. McCrea M, Prichep LS, Powell MR, et al. Acute effects and recovery after sport-related concussion: a neurocognitive and quantitative brain electrical activity study.
J. Head Trauma Rehabil. 2010; 25:283–92.
67. Patricios J, Fuller GW, Ellenbogen RG, et al. What are the critical elements of sideline screening that can be used to establish the diagnosis of concussion? A systematic review.
Br. J. Sports Med. 2017; 51:888–94.
68. Raynowska J, Hasanaj L, Zhang I. Agreement of the spiral-bound and computerized tablet versions of the King-Devick test of rapid number naming for sports concussion.
Ann. Sports Med. Res. 2015; 2:1051.
69. King D, Gissane C, Hume PA, Flaws M. The King-Devick test was useful in management of concussion in amateur rugby union and rugby league in New Zealand.
J. Neurol. Sci. 2015; 351:58–64.
70. Galetta KM, Liu M, Leong DF, et al. The King-Devick test of rapid number naming for concussion detection: meta-analysis and systematic review of the literature.
Concussion. 2016; 1.
71. Ghosh Hajra S, Liu CC, Song X, et al. Developing brain vital signs: initial framework for monitoring brain function changes over time.
Front. Neurosci. 2016; 10:211.
72. Ghosh Hajra S. Multimodal characterization of the semantic N400 response within a rapid evaluation brain vital sign framework.
J. Transl. Med. 2018; 16:151.
73. Daley M, Dekaban G, Bartha R, et al. Metabolomics profiling of concussion in adolescent male hockey players: a novel diagnostic method.
Metabolomics. 2016; 12:185.
74. Zhou Y, Kierans A, Kenul D, et al. Mild traumatic brain injury: longitudinal regional brain volume changes.
Radiology. 2013; 267:880–90.
75. Lipton ML, Kim N, Zimmerman ME, et al. Soccer heading is associated with white matter microstructural and cognitive abnormalities.
Radiology. 2013; 268:850–7.
76. Huang M-X, Theilmann RJ, Robb A, et al. Integrated imaging approach with MEG and DTI to detect mild traumatic brain injury in military and civilian patients.
J. Neurotrauma. 2009; 26:1213–26.
77. Alford PW, Dabiri BE, Goss JA, et al. Blast-induced phenotypic switching in cerebral vasospasm.
Proc. Natl. Acad. Sci. 2011; 108:12705–10.
78. Hemphill MA, Dabiri BE, Gabriele S, et al. A possible role for integrin signaling in diffuse axonal injury.
PLoS One. 2011; 6:e22899.
79. Kilinc D, Gallo G, Barbee KA. Mechanically-induced membrane poration causes axonal beading and localized cytoskeletal damage.
Exp. Neurol. 2008; 212:422–30.
80. LaPlaca MC, Cullen DK, McLoughlin JJ, Cargill RS. High rate shear startin of three-dimensional neural cell cultures: a new in vitro traumatic brain injury model.
J. Biomech. 2005; 38:1093–105.
81. Montenigro PH, Alosco ML, Martin BM, et al. Cumulative head impact exposure predicts later-life depression, apathy, executive dysfunction, and cognitive impairment in former high school and college football players.
J. Neurotrauma. 2017; 34:328–40.
82. Greenwald RM, Gwin JT, Chu JJ, Crisco JJ. Head impact severity measures for evaluating mild traumatic brain injury risk exposure.
Neurosurgery. 2008; 62:789–98.
83. Broglio SP, Lapointe A, O’Connor KL, McCrea M. Head impact density: a model to explain the elusive concussion threshold.
J. Neurotrauma. 2017; 34:2675–83.
84. Allison MA, Kang YS, Maltese MR, et al. Measurement of Hybrid III head impact kinematics using an accelerometer and gyroscope system in ice hockey helmets.
Ann. Biomed. Eng. 2015; 43:1896–906.
85. Young TJ, Daniel RW, Rowson S, Duma SM. Head impact exposure in youth football: elementary school ages 7-8 years and the effect of returning players.
Clin. J. Sport Med. 2014; 24:416–21.
86. Margulies SS, Kilbaugh T, Sullivan S, et al. Establishing a clinically relevant large animal model platform for TBI therapy development: using cyclosporin a as a case study.
Brain Pathol. 2015; 25:289–303.
87. Hoffer BJ, Pick CG, Hoffer ME, et al. Repositioning drugs for traumatic brain injury—N-acetyl cysteine and phenserine.
J. Biomed. Sci. 2017; 24:71.
88. Ferrari MD, Klever RR, Terwindt GM, et al. Migraine pathophysiology: lessons from mouse models and human genetics.
Lancet. Neurol. 2015; 14:65–80.
89. Hoffer ME, Balaban C, Slade MD, et al. Amelioration of acute sequelae of blast induced mild traumatic brain injury by N-acetyl cysteine: a double-blind, placebo controlled study.
PLoS One. 2013; 8:e54163.
90. Baratz-Goldstein R, Deselms H, Heim LR, et al. Thioredoxin-mimetic-peptides protect cognitive function after mild traumatic brain injury (mTBI).
PLoS One. 2016; 11:e0157064.
91. Ji X, Peng D, Zhang Y, et al. Astaxanthin improves cognitive performance in mice following mild traumatic brain injury.
Brain Res. 2017; 1659:88–95.
92. Mills JD, Bailes JE, Sedney CL, et al. Omega-3 fatty acid supplementation and reduction of traumatic axonal injury in a rodent head injury model.
J. Neurosurg. 2011; 114:77–84.
93. McCrory P, Meeuwisse W, Johnston K, et al. Consensus statement on concussion in sport—the 3rd International Conference on Concussion in Sport, held in Zurich, November 2008.
J. Clin. Neurosci. 2009; 16:755–63.
94. Bailes JE, Patel V. The potential for DHA to mitigate mild traumatic brain injury.
Mil. Med. 2014; 179(Suppl 11):112–6.
95. Sakellaris G, Nasis G, Kotsiou M, et al. Prevention of traumatic headache, dizziness and fatigue with creatine administration. A pilot study.
Acta. Paediatr. 2008; 97:31–4.
96. Tang H, Hua F, Wang J, et al. Progesterone and vitamin D combination therapy modulates inflammatory response after traumatic brain injury.
Brain Inj. 2015; 29:1165–74.
97. LeBlanc ES, Perrin N, Johnson JD Jr., et al. Over-the-counter and compounded vitamin D: is potency what we expect?
JAMA Intern. Med. 2013; 173:585–6.
98. Polak P, Leddy JJ, Dwyer MG, et al. Diffusion tensor imaging alterations in patients with postconcussion syndrome undergoing exercise treatment: a pilot longitudinal study.
J. Head Trauma Rehabil. 2015; 30(2):E32–42.
99. Leddy JJ, Willer B. Use of graded exercise testing in concussion and return-to-activity management.
Curr. Sports Med. Rep. 2013; 12:370–6.
100. Schneider KJ, Leddy JJ, Guskiewicz KM, et al. Rest and treatment/rehabilitation following sport-related concussion: a systematic review.
Br. J. Sports Med. 2017; 51(2):930–4.
101. Leddy JJ, Hinds AL, Miecznikowski JC, et al. Safety and prognostic utility of provocative exercise testing in acutely concussed adolescents: a randomized trial.
Clin. J. Sport Med. 2018; 28:13–20.
102. Bloodgood B, Inokuchi D, Shawver W, et al. Exploration of awareness, knowledge, and perceptions of traumatic brain injury among American youth athletes and their parents.
J. Adolesc. Health. 2013; 53:34–9.
103. Brenner JS, Council on Sports Medicine and Fitness. Sports specialization and intensive training in young athletes.
Pediatrics 2016; 138. pii e20162148. Epub 2016/08/31.
104. Minnesota Hockey. Minnesota hockey breaks record for 8 and under players 2017. September 13, 2017. [cited 2018 Nov 6]. Available from:
https://www.minnesotahockey.org/news_article/show/804154.
105. NFHS. High school sports participation increases for 28th straight year, nears 8 million mark. September 13, 2017. [cited 2018 Nov 6]. Available from:
https://www.nfhs.org/articles/high-school-sports-participation-increases-for-28th-straight-year-nears-8-million-mark/.
106. Bandura A, Ross D, Ross SA. Transmission of aggression through imitation of aggressive models.
J. Abnorm. Soc. Psychol. 1961; 63:575–82.
107. Patricios J. Implementation of the 2017 Berlin Concussion in Sport Group Consensus Statement in Contact and Collision Sports: a joint position statement from 11 national and international sport organisations.
Br. J. Sports Med. 2018:635–41.
108. Shen FX. Are youth sports concussion statutes working.
Duq L Rev. 2018; 56:7.
