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Emilie Chamard, Hugo Théoret, Elaine N. Skopelja, Lorie A. Forwell, Andrew M. Johnson and Paul S. Echlin

Object

Despite negative neuroimaging findings using traditional neuroimaging methods such as MRI and CT, sports-related concussions have been shown to cause neurometabolic changes in both the acute and subacute phases of head injury. However, no prospective clinical study has used an independent physician-observer design in the monitoring of these changes. The objective of this study was to evaluate the effects of repetitive concussive and sub-concussive head impacts on neurometabolic concentrations in a prospective study of two Canadian Interuniversity Sports (CIS) ice hockey teams using MR spectroscopy (MRS).

Methods

Forty-five ice hockey players (25 men and 20 women) participated in this study. All participants underwent pre- and postseason MRI, including spectroscopy imaging, using a 3-T MRI machine. The linear combination model was used to quantify the following ratios: glutamate/creatine-phosphocreatine (Cr), myoinositol/Cr, and N-acetylaspartate (NAA)/Cr. Individuals sustaining a medically diagnosed concussion were sent for MRI at 72 hours, 2 weeks, and 2 months after injury.

Results

No statistically significant differences were observed between athletes who were diagnosed with a concussion and athletes who were not clinically diagnosed as sustaining a concussion. Although no statistically significant longitudinal metabolic changes were observed among athletes who were diagnosed with a concussion, the results demonstrated a predictable pattern of initial impairment, followed by a gradual return to ratios that were similar to, but lower than, baseline ratios. No significant pre- to postseason changes were demonstrated among men who were not observed to sustain a concussion. However, a substantively significant decrease in the NAA/Cr ratio was noted among the female hockey players (t(13) = 2.58, p = 0.02, η2 = 0.34).

Conclusions

A key finding in this study, from the standpoint of future research design, is the demonstration of substantively significant metabolic changes among the players who were not diagnosed with a concussion. In addition, it may explain why there are few statistically significant differences demonstrated between players who were diagnosed with a concussion and players who were not diagnosed with a concussion (that is, the potency of the independent variable was diminished by the fact that the group of players not diagnosed with a concussion might be better described as a subgroup of the players who may have sustained a concussion but were not observed and diagnosed with a concussion). This result suggests that definitions of concussion may need to be revisited within sports with high levels of repetitive subconcussive head impacts. Future analysis of these data will examine the relationships between the modes of MRI (diffusion tensor imaging, MRS, and susceptibility-weighted MR imaging) used in this study, along with other more sensitive evaluative techniques. This type of intermodal comparison may improve the identification of concussions that were previously dependent on the unreliable self-reporting of recognized concussion symptomatology by the athlete or on poorly validated neuropsychological tests.

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Paul S. Echlin, Elaine N. Skopelja, Rachel Worsley, Shiroy B. Dadachanji, D. Rob Lloyd-Smith, Jack A. Taunton, Lorie A. Forwell and Andrew M. Johnson

Object

The primary objective of this study was to measure the incidence of concussion according to a relative number of athlete exposures among 25 male and 20 female varsity ice hockey players. The secondary objective was to present neuropsychological test results between preseason and postseason play and at 72 hours, 2 weeks, and 2 months after concussion.

Methods

Every player underwent baseline assessments using the Sport Concussion Assessment Tool-2 (SCAT2), Immediate Post-Concussion Assessment and Cognitive Test (ImPACT), and MRI. Each regular season and postseason game was observed by 2 independent observers (a physician and a nonphysician observer). Players with a diagnosed concussion were removed from the game, examined in the team physician's office using the SCAT2 and ImPACT, and sent to undergo MRI.

Results

Eleven concussions occurred during the 55 physician-observed games (20%). The incidence of concussion, expressed as number of concussions per 1000 athlete exposures, was 10.70 for men and women combined in regular season play, 11.76 for men and women combined across both the regular season and playoff season, 7.50 for men and 14.93 for women in regular season play, and 8.47 for men across both the regular season and playoff season. One male player experienced repeat concussions. No concussions were reported during practice sessions, and 1 concussion was observed and diagnosed in an exhibition game. Neuropsychological testing suggested no statistically significant preseason/postseason differences between athletes who sustained a physician-diagnosed concussion and athletes who did not sustain a physician-diagnosed concussion on either the ImPACT or SCAT2. The athletes who sustained a physician-diagnosed concussion demonstrated few reliable changes postinjury.

Conclusions

Although the incidence of game-related concussions per 1000 athlete exposures in this study was half the highest rate reported in the authors' previous research, it was 3 times higher than the incidence reported by other authors within the literature concerning men's collegiate ice hockey and 5 times higher than the highest rate previously reported for woman's collegiate ice hockey. Interestingly, the present results suggest a substantively higher incidence of concussion among women (14.93) than men (7.50). The reproducible and significantly higher incidence of concussion among both men and woman ice hockey players, when compared with nonphysician-observed games, suggests a significant underestimation of sports concussion in the scientific literature.

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Paul Sean Echlin, Charles H. Tator, Michael D. Cusimano, Robert C. Cantu, Jack E. Taunton, Ross E. G. Upshur, Craig R. Hall, Andrew M. Johnson, Lorie A. Forwell and Elaine N. Skopelja

Object

The objective of this study was to measure the incidence of concussion (scaled relative to number of athlete exposures) and recurrent concussion within 2 teams of fourth-tier junior ice hockey players (16–21 years old) during 1 regular season.

Methods

A prospective cohort study called the Hockey Concussion Education Project was conducted during 1 junior ice hockey regular season (2009–2010) involving 67 male fourth-tier ice hockey players (mean age 18.2 ± 1.2 years, range 16–21 years) from 2 teams. Prior to the start of the season, every player underwent baseline assessments using the Sideline Concussion Assessment Tool 2 (SCAT2) and the Immediate Post-Concussion Assessment and Cognitive Test (ImPACT). The study protocol also required players who entered the study during the season to complete baseline SCAT2 and ImPACT testing. If the protocol was not followed, the postinjury test results of a player without true baseline test results would be compared against previously established age and gender group normative levels. Each regular season game was observed by a qualified physician and at least 1 other neutral nonphysician observer. Players who suffered a suspected concussion were evaluated at the game. If a concussion diagnosis was made, the player was subsequently examined in the physician's office for a full clinical evaluation and the SCAT2 and ImPACT were repeated. Based on these evaluations, players were counseled on the decision of when to return to play. Athlete exposure was defined as 1 game played by 1 athlete.

Results

Twenty-one concussions occurred during the 52 physician-observed games (incidence 21.5 concussions per 1000 athlete exposures). Five players experienced repeat concussions. No concussions were reported during practice sessions. A concussion was diagnosed by the physician in 19 (36.5%) of the 52 observed games. One of the 5 individuals who suffered a repeat concussion sustained his initial concussion in a regular season game that was not observed by a physician, and as a result this single case was not included in the total of 21 total concussions. This initial concussion of the player was identified during baseline testing 2 days after the injury and was subsequently medically diagnosed and treated.

Conclusions

The incidence of game-related concussions (per 100 athlete exposures) in these fourth-tier junior ice hockey players was 7 times higher than the highest rate previously reported in the literature. This difference may be the result of the use of standardized direct physician observation, diagnosis, and subsequent treatment. The results of this study demonstrate the need for follow-up studies involving larger and more diverse sample groups to reflect generalizability of the findings. These follow-up studies should involve other contact sports (for example football and rugby) and also include the full spectrum of gender, age, and skill levels.

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Paul Sean Echlin, Charles H. Tator, Michael D. Cusimano, Robert C. Cantu, Jack E. Taunton, Ross E. G. Upshur, Michael Czarnota, Craig R. Hall, Andrew M. Johnson, Lorie A. Forwell, Molly Driediger and Elaine N. Skopelja

Object

The authors investigated return-to-play duration for initial and recurrent concussion in the same season in 2 teams of junior (16–21-year-old) ice hockey players during a regular season.

Methods

The authors conducted a prospective cohort study during 1 junior regular season (2009–2010) of 67 male fourth-tier ice hockey players (mean age 18.2 ± 1.2 years [SD], range 16–21 years) from 2 teams.

Prior to the start of the season, every player underwent baseline assessments that were determined using the Sideline Concussion Assessment Tool 2 (SCAT2) and the Immediate Post-Concussion Assessment and Cognitive Test (ImPACT). The study protocol also required players who entered the study during the season to complete a baseline SCAT2 and ImPACT. If the protocol was not followed, the postinjury test results of a player without true baseline test results were compared with previously established age- and sex-matched group normative levels.

Each game was directly observed by a physician and at least 1 neutral nonphysician observer. Players suspected of suffering a concussion were evaluated by the physician during the game. If a concussion was diagnosed, the player underwent clinical evaluation at the physician's office within 24 hours.

The return-to-play decision was based on clinical evaluation guided by the Zurich return-to-play protocol (contained in the consensus statement of international expert opinion at the 3rd International Conference on Concussion in Sport held in Zurich, November 2008). This clinical evaluation and return-to-play protocol was augmented by the 2 tests (SCAT2 and ImPACT) also recommended by the Zurich consensus statement, for which baseline values had been obtained.

Results

Seventeen players sustained a physician-observed or self-reported, physician-diagnosed concussion during a physician-observed ice hockey game. The mean clinical return-to-play duration (in 15 cases) was 12.8 ± 7.02 days (median 10 days, range 7–29 days); the mean number of physician office visits by players who suffered a concussion (15 cases) was 2.1 ± 1.29 (median 1.5 visits). Five of the 17 players who sustained a concussion also suffered a recurrent or second concussion. One of the 5 individuals who suffered a repeat concussion sustained his initial concussion in a regular season game that was not observed by a physician, and as a result this single case was not included in the total of 21 concussions. This initial concussion of the player was identified during baseline testing 2 days after the injury and was subsequently medically diagnosed and treated. The mean interval between the first and second concussions in these 5 players was 78.6 ± 39.8 days (median 82 days), and the mean time between the return-to-play date of the first and second concussions was 61.8 ± 39.7 days (median 60 days).

Conclusions

The mean rates of return to play for single and recurrent concussions were higher than rates cited in recent studies involving sport concussions. The time interval between the first and second concussions was also greater than previously cited. This difference may be the result of the methodology of direct independent physician observation, diagnosis, and adherence to the Zurich return-to-play protocol.

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Paul Sean Echlin, Andrew M. Johnson, Suzanne Riverin, Charles H. Tator, Robert C. Cantu, Michael D. Cusimano, Jack E. Taunton, Ross E. G. Upshur, Craig R. Hall, Lorie A. Forwell and Elaine N. Skopelja

Object

The aim of this study was to evaluate the effectiveness of an educational intervention on concussion knowledge within a sample of junior fourth-tier ice hockey players.

Methods

A prospective cohort study, called the Hockey Concussion Education Project, was conducted during 1 junior ice hockey regular season (2009–2010) with 67 male fourth-tier ice hockey players (mean age 18.2 ± 1.2 years, range 16–21 years) from 2 teams. All participating players were randomized into 3 concussion education intervention groups (DVD group, interactive computer module [ICM] group, or control group) before the beginning of the season. Each individual received a preintervention knowledge test prior to the intervention. The DVD and ICM groups received a posttest after the completion of their intervention. All participants were offered the same knowledge test at 15 games (50 days) and 30 games (91 days) later.

Results

In the concussion education intervention component no significant group differences were observed at baseline between individuals in the control group and between individuals within the interventional group. At the 15-game follow-up, however, the difference between groups approached significance (F [1, 30] = 3.91, p = 0.057). This group difference remained consistent at the 30-game follow-up.

Conclusions

This study demonstrates a positive trend concerning concussion education intervention and knowledge acquisition with either the ICMs or the educational DVD. Both forms of intervention produced a positive and sustainable improvement that approached statistical significance when compared with the control group. The control group demonstrated a negative longitudinal trend concerning concussion knowledge.

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Karl G. Helmer, Ofer Pasternak, Eli Fredman, Ronny I. Preciado, Inga K. Koerte, Takeshi Sasaki, Michael Mayinger, Andrew M. Johnson, Jeffrey D. Holmes, Lorie A. Forwell, Elaine N. Skopelja, Martha E. Shenton and Paul S. Echlin

Object

Concussion, or mild traumatic brain injury (mTBI), is a commonly occurring sports-related injury, especially in contact sports such as hockey. Cerebral microbleeds (CMBs), which appear as small, hypointense lesions on T2*-weighted images, can result from TBI. The authors use susceptibility-weighted imaging (SWI) to automatically detect small hypointensities that may be subtle signs of chronic and acute damage due to both subconcussive and concussive injury. The goal was to investigate how the burden of these hypointensities changes over time, over a playing season, and postconcussion, in comparison with subjects who did not suffer a medically observed and diagnosed concussion.

Methods

Images were obtained in 45 university-level adult male and female ice hockey players before and after a single Canadian Interuniversity Sports season. In addition, 11 subjects (5 men and 6 women) underwent imaging at 72 hours, 2 weeks, and 2 months after concussion. To identify subtle changes in brain tissue and potential CMBs, nonvessel clusters of hypointensities on SWI were automatically identified, and a hypointensity burden index was calculated for all subjects at the beginning of the season (BOS), the end of the season (EOS), and at postconcussion time points (where applicable).

Results

A statistically significant increase in the hypointensity burden, relative to the BOS, was observed for male subjects with concussions at the 2-week postconcussion time point. A smaller, nonsignificant rise in the burden for female subjects with concussions was also observed within the same time period. There were no significant changes in burden for nonconcussed subjects of either sex between the BOS and EOS time points. However, there was a statistically significant difference in the burden between male and female subjects in the nonconcussed group at both the BOS and EOS time points, with males having a higher burden.

Conclusions

This method extends the utility of SWI from the enhancement and detection of larger (> 5 mm) CMBs, which are often observed in more severe cases of TBI, to cases involving smaller lesions in which visual detection of injury is difficult. The hypointensity burden metric proposed here shows statistically significant changes over time in the male subjects. A smaller, nonsignificant increase in the burden metric was observed in the female subjects.

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Ofer Pasternak, Inga K. Koerte, Sylvain Bouix, Eli Fredman, Takeshi Sasaki, Michael Mayinger, Karl G. Helmer, Andrew M. Johnson, Jeffrey D. Holmes, Lorie A. Forwell, Elaine N. Skopelja, Martha E. Shenton and Paul S. Echlin

Object

Concussion is a common injury in ice hockey and a health problem for the general population. Traumatic axonal injury has been associated with concussions (also referred to as mild traumatic brain injuries), yet the pathological course that leads from injury to recovery or to long-term sequelae is still not known. This study investigated the longitudinal course of concussion by comparing diffusion MRI (dMRI) scans of the brains of ice hockey players before and after a concussion.

Methods

The 2011–2012 Hockey Concussion Education Project followed 45 university-level ice hockey players (both male and female) during a single Canadian Interuniversity Sports season. Of these, 38 players had usable dMRI scans obtained in the preseason. During the season, 11 players suffered a concussion, and 7 of these 11 players had usable dMRI scans that were taken within 72 hours of injury. To analyze the data, the authors performed free-water imaging, which reflects an increase in specificity over other dMRI analysis methods by identifying alterations that occur in the extracellular space compared with those that occur in proximity to cellular tissue in the white matter. They used an individualized approach to identify alterations that are spatially heterogeneous, as is expected in concussions.

Results

Paired comparison of the concussed players before and after injury revealed a statistically significant (p < 0.05) common pattern of reduced free-water volume and reduced axial diffusivity and fractional anisotropy following elimination of freewater. These free-water–corrected measures are less affected by partial volumes containing extracellular water and are therefore more specific to processes that occur within the brain tissue. Fractional anisotropy was significantly increased, but this change was no longer significant following the free-water elimination.

Conclusions

Concussion during ice hockey games results in microstructural alterations that are detectable using dMRI. The alterations that the authors found suggest decreased extracellular space and decreased diffusivities in white matter tissue. This finding might be explained by axonal injury and/or by increased cellularity of glia cells. Even though these findings in and of themselves cannot determine whether the observed microstructural alterations are related to long-term pathology or persistent symptoms, they are important nonetheless because they establish a clearer picture of how the brain responds to concussion.

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Takeshi Sasaki, Ofer Pasternak, Michael Mayinger, Marc Muehlmann, Peter Savadjiev, Sylvain Bouix, Marek Kubicki, Eli Fredman, Brian Dahlben, Karl G. Helmer, Andrew M. Johnson, Jeffrey D. Holmes, Lorie A. Forwell, Elaine N. Skopelja, Martha E. Shenton, Paul S. Echlin and Inga K. Koerte

Object

The aim of this study was to examine the brain's white matter microstructure by using MR diffusion tensor imaging (DTI) in ice hockey players with a history of clinically symptomatic concussion compared with players without a history of concussion.

Methods

Sixteen players with a history of concussion (concussed group; mean age 21.7 ± 1.5 years; 6 female) and 18 players without a history of concussion (nonconcussed group; mean age 21.3 ± 1.8 years, 10 female) underwent 3-T DTI at the end of the 2011–2012 Canadian Interuniversity Sports ice hockey season. Tract-based spatial statistics (TBSS) was used to test for group differences in fractional anisotropy (FA), axial diffusivity (AD), radial diffusivity (RD), and the measure “trace,” or mean diffusivity. Cognitive evaluation was performed using the Immediate Postconcussion Assessment and Cognitive Test (ImPACT) and the Sport Concussion Assessment Tool–2 (SCAT2).

Results

TBSS revealed a significant increase in FA and AD, and a significant decrease in RD and trace in several brain regions in the concussed group, compared with the nonconcussed group (p < 0.05). The regions with increased FA and decreased RD and trace included the right posterior limb of the internal capsule, the right corona radiata, and the right temporal lobe. Increased AD was observed in a small area in the left corona radiata. The DTI measures correlated with neither the ImPACT nor the SCAT2 scores.

Conclusions

The results of the current study indicate that a history of concussion may result in alterations of the brain's white matter microstructure in ice hockey players. Increased FA based on decreased RD may reflect neuroinflammatory or neuroplastic processes of the brain responding to brain trauma. Future studies are needed that include a longitudinal analysis of the brain's structure and function following a concussion to elucidate further the complex time course of DTI changes and their clinical meaning.

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Paul S. Echlin, Andrew M. Johnson, Jeffrey D. Holmes, Annalise Tichenoff, Sarah Gray, Heather Gatavackas, Joanne Walsh, Tim Middlebro, Angelique Blignaut, Martin MacIntyre, Chris Anderson, Eli Fredman, Michael Mayinger, Elaine N. Skopelja, Takeshi Sasaki, Sylvain Bouix, Ofer Pasternak, Karl G. Helmer, Inga K. Koerte, Martha E. Shenton and Lorie A. Forwell

Current research on concussion is primarily focused on injury identification and treatment. Prevention initiatives are, however, important for reducing the incidence of brain injury. This report examines the development and implementation of an interactive electronic teaching program (an e-module) that is designed specifically for concussion education within an adolescent population. This learning tool and the accompanying consolidation rubric demonstrate that significant engagement occurs in addition to the knowledge gained among participants when it is used in a school curriculum setting.