Return to play after an initial or recurrent concussion in a prospective study of physician-observed junior ice hockey concussions: implications for return to play after a concussion

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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.

Abbreviations used in this paper: HCEP = Hockey Concussion Education Project; ImPACT = Immediate Post-Concussion Assessment and Cognitive Test; MBESS = Modified Balance Error Scoring System; SAC = Standardized Assessment of Concussion; SCAT2 = Sideline Concussion Assessment Tool 2.

Abstract

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.

The direct independent medical assessment and protocol-guided return to play after an athlete has sustained a medically diagnosed concussion is believed to be essential in the acute concussion care.19,23 This approach may decrease the frequency of short- and long-term sequelae (such as postconcussion syndrome; mild cognitive impairment; chronic traumatic encephalopathy) related to this injury.4,5,8,9,19,20,22,25,26 It may also improve the return-to-play data on which individual decisions are determined. Previously published return-to-play concussion-focused studies have been difficult to compare, as they have been based on different surveillance and return-to-play protocols.1,10,12,14–16,18,24,28

The primary goal of the present study was to prospectively measure the duration of medical restriction from play (return-to-play period) after each physician-observed and -diagnosed concussion or recurrent concussion, by direct clinical evaluation augmented with the SCAT2 and ImPACT neuropsychological tools. We studied players from 2 teams of junior ice hockey players during a single regular (36-game) season using the Zurich return-to-play protocol.19

Methods

This study was part of a larger surveillance and reporting study also published in this issue.6 The experimental sample described herein was collected during the 2009–2010 junior ice hockey regular season, and it included 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 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. Mean results are presented ± the SD.

For a complete and detailed description of the methods used in the HCEP please see Echlin and colleagues' article, “A prospective study of physician-observed concussions during junior ice hockey: implications for incidence rates,” in this issue of Neurosurgical Focus.6

Results

In 15 players who suffered a concussion, the mean interval before clinical return to play was 12.8 ± 7.02 days (median 10 days, range 7–29 days); the mean number of physician office visits by 15 players who suffered a concussion was 2.1 ± 1.29 (median 1.5 visits).

These calculations exclude 1 player (an outlier who was out for the season and did not return to play [more than 75 days]), 5 players who refused follow-up, and 4 HCEP players with a physician-diagnosed concussion in whom the event had occurred outside the parameters of the study (2 players in the first round of the playoffs and 2 players in games that were not being observed).

The mean return-to-play duration of players with a reported medical history of concussion were as follows: 11.5 ± 7.60 days in 8 players with 0 previous concussions; 10.7 ± 2.94 days in 6 players with 1–2 previous concussions; more than 28 days in players with more than 3 previous concussions (1 case) (excluding the 1 outlier player and the 5 players who refused to follow-up with the physician).

Eighteen (53%) of the 34 potential concussions identified by the physician and nonphysician observers were positively diagnosed by the physician at rinkside. Three of the diagnosed concussions were not directly identified in an observed game, and were self-reported to the physician either at rinkside or within the next 48 hours. The remaining 16 (47%) of the concussions that were initially identified by the observers were returned to play after a negative clinical and SCAT2 evaluation by the physician.

Five (29%) of 17 players who suffered a concussion also sustained a recurrent concussion during that interval. 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 span between the return-to-play date of the first and second concussions was 61.8 ± 39.7 days (median 60 days).

The concussion diagnosis and return-to-play decision of the athlete were augmented by the use of the ImPACT and the SCAT2. The linear neurocognitive recovery trend over time (number of office visits) of the SCAT2 symptoms, the SAC score, and the Modified BESS score are presented in Figs. 13.

Fig. 1.
Fig. 1.

Graph demonstrating change of the SCAT2 symptom inventory total during the recovery period.

Fig. 2.
Fig. 2.

Graph showing SCAT2 SAC total scores for concussed athletes during the recovery period.

Fig. 3.
Fig. 3.

Graph demonstrating changes of SCAT2 Modified BESS total scores for concussed athletes during the recovery period.

Discussion

This is the first study to use independent on-site physicians to diagnose and then determine a player's return-to play status according to the Zurich protocol.19 Among the published concussion studies, the lack of a single standardized methodology involving documentation of return to play makes direct comparison of results difficult and allows only trends to be discussed.

In the present study, the mean clinical return-to-play duration of the participants who suffered a new or recurrent concussion during the observed season was 12.8 days. Seven (33%) of the 21 athletes diagnosed with a concussion required more than 12.8 days before returning to play. This calculation includes 2 players who were unable to return to play for the rest of the season due to ongoing symptoms. Previous studies have demonstrated that athletes tend to recover from perceived symptoms and their neurocognitive performance normalizes within 3–10 days, with a smaller percentage of individuals that require more time to recover.1,12,14–16,18

Previous studies have also demonstrated that players who sustained a concussion in a season were 3 times more likely to sustain a second concussion in the same season compared with uninjured players.11,29 Five (29%) of 17 players who sustained a concussion in this study also sustained a second concussion in the same season. Three of these 5 players who suffered a repeat concussion had a medical history of sustaining at least 1 concussion prior to the beginning of the season.

The mean clinical return-to-play duration for individuals who reported never previously suffering a concussion before the start of the observed season (8 players) was 11.5 days; this value was greater than the mean clinical return-to-play duration (10.7 ± 2.94 days) for individuals (6 players) who reported having between 1 and 2 previous concussions.

The literature documents lengthened recovery times in individuals who reported suffering 3 or more prior concussions.3,7,10,13 There were 2 HCEP players who reported 3 or more previous concussions and who sustained a concussion during the study. In both players a significantly longer duration for recovery from symptoms and objective neurocognitive measurements was demonstrated. One player, who reported 5 previous concussions, had a significantly longer return-to-play duration (28 days), and the second player who reported 4 previous concussions was unable to return to play and had to retire permanently due to ongoing symptoms. Individual concussion history data may be underreported due to individual bias and to the interpretation of the definition of concussion.

Recurrent concussions may be related to the fact that players are often prematurely returned to play.24,28 This was not found in the results of the HCEP, as the mean interval between the first and second concussions in the same season (in 5 players) was 78.6 ± 39.8 days (median 82 days). These results differ from the 10-day period in which the second or recurrent concussion most frequently occurred in previous studies.10,17 The difference in these findings may be attributable to the direct surveillance and strict adherence to the Zurich return-to-play protocol used in the HCEP, and the small sample size used in this study.

The present study used neurocognitive tools such as SCAT2 and ImPACT to augment clinical decision making. These tools should not be considered independent decision-making instruments. Rather, they can supplement clinical information but not override physician judgment. In 8 (38%) of 21 cases of concussions diagnosed and sequentially followed, the athletes scored either in the normal range or within their baseline ImPACT score but were clearly still symptomatic. In 2 (10%) of 21 concussions evaluated, the player would be symptom free and would exhibit cognitive deficits on SCAT2 or ImPACT. These findings of inconsistent results in the objective neuropsychological tools may be attributed to operator error, the learning effect of the participant athlete, or the lack of sensitivity of the test itself.24,27

This study concurs with previous studies in the literature that conclude that there is currently no single direct measure of recovery after concussion and that clinical decisions should be made based on multifactorial input including concussion history, symptoms, balance, and cognitive function.2,14,21

A limitation of this study was the lack of compliance of HCEP participants with objective baseline testing and retesting at the requested intervals. Although general trends in the objective testing data demonstrated the utility of the objective testing tools, the lack of participant compliance made it difficult to document a complete data set of the objective measurements for comparison purposes. A second limitation of this study was the absence of a matched control group of individuals not involved with the participating teams.

Future studies should focus on improved compliance of participant baseline and postinjury testing. The complete SCAT2 data should be collected and compared across the population to assist in validating and improving this screening tool compared with the components that were used in this study. Future studies should also be performed in larger populations, in other contact sports, across sex, across different levels of play, and across different countries to assess the generalizability of these findings.

Conclusions

The mean rate of return to play after a single and recurrent concussion was higher than the rate in recent studies involving sports-related concussions. The interval between the first and second concussions was also greater than previously cited. This difference may be a result of the present methodology, including independent direct physician observation and adherence to the Zurich return-to-play protocol.

Disclosure

This work was funded by the Ontario Trillium Foundation, the Dr. Tom Pashby Safety Fund, and the Dave Irwin Foundation for Brain Injury. The Ontario Neurotrauma Foundation is acknowledged for its administrative and facilitative contributions. Dr. Cusimano is funded by the Canadian Institutes of Health Strategic Teams in Applied Injury Research.

The opinions contained herein are those of the authors and not necessarily of the organizations funding the research.

Author contributions to the study and manuscript preparation include the following. Conception and design: all authors. Acquisition of data: Echlin, Hall. Analysis and interpretation of data: Echlin, Tator, Cusimano, Cantu, Taunton, Czarnota, Hall, Johnson, Forwell. Drafting the article: Echlin, Tator, Cusimano, Cantu, Czarnota, Hall, Forwell, Skopelja. Critically revising the article: all authors. Reviewed final version of the manuscript and approved it for submission: all authors. Statistical analysis: Echlin, Johnson. Administrative/technical/material support: Tator, Forwell, Driediger, Skopelja. Study supervision: Echlin, Hall, Forwell.

Acknowledgments

The authors would like to acknowledge the contributions of the members of the Hockey Concussion Education Project Team: Michael A. Czarnota, Ph.D., Wayne State University, Detroit, Michigan; Suzanne Riverin, Ph.D., Nipissing University, North Bay, Ontario, Canada; the Hockey Neurotrauma and Concussion Initiative Research Committee; and the editorial work of Kim Echlin, Ph.D., University of Toronto, Ontario, Canada.

The authors would like to acknowledge the players and staffs of Team A and Team B for their participation in the HCEP. They would also like to acknowledge the participating physicians, observers, and volunteers for their contributions to the HCEP.

References

  • 1

    Bleiberg JCernich ANCameron KSun WPeck KEcklund PJ: Duration of cognitive impairment after sports concussion. Neurosurgery 54:107310802004

  • 2

    Broglio SPSosnoff JJFerrara MS: The relationship of athlete-reported concussion symptoms and objective measures of neurocognitive function and postural control. Clin J Sport Med 19:3373822009

  • 3

    Collins MWLovell MRIverson GLCantu RCMaroon JCField M: Cumulative effects of concussion in high school athletes. Neurosurgery 51:117511812002

  • 4

    De Beaumont LLassonde MLeclerc SThéoret H: Long-term and cumulative effects of sports concussion on motor cortex inhibition. Neurosurgery 61:3293372007

  • 5

    De Beaumont LThéoret HMongeon DMessier JLeclerc STremblay S: Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 132:6957082009

  • 6

    Echlin PSTator CHCusimano MDCantu RCTaunton JEUpshur REG: A prospective study of physician-observed concussions during junior ice hockey: implications for incidence rates. Neurosurg Focus 29:5E42010

  • 7

    Gaetz MGoodman DWeinberg H: Electrophysiological evidence for the cumulative effects of concussion. Brain Inj 14:107710882000

  • 8

    Guskiewicz KMMarshall SWBailes JMcCrea MCantu RCRandolph C: Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery 57:7197262005

  • 9

    Guskiewicz KMMarshall SWBailes JMcCrea MHarding HP JrMatthews A: Recurrent concussion and risk of depression in retired professional football players. Med Sci Sports Exerc 39:9039092007

  • 10

    Guskiewicz KMMcCrea MMarshall SWCantu RCRandolph CBarr W: Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 290:254925552003

  • 11

    Guskiewicz KMWeaver NLPadua DAGarrett WE Jr: Epidemiology of concussion in collegiate and high school football players. Am J Sports Med 28:6436502000

  • 12

    Iverson GLBrooks BLCollins MWLovell MR: Tracking neuropsychological recovery following concussion in sport. Brain Inj 20:2452522006

  • 13

    Iverson GLGaetz MLovell MRCollins MW: Cumulative effects of concussion in amateur athletes. Brain Inj 18:4334432004

  • 14

    Macciocchi SNBarth JTAlves WRimel RWJane JA: Neuropsychological functioning and recovery after mild head injury in collegiate athletes. Neurosurgery 39:5105141996

  • 15

    Makdissi MMcCrory PUgoni ADarby DBrukner P: A prospective study of postconcussive outcomes after return to play in Australian football. Am J Sports Med 37:8778832009

  • 16

    McCrea MGuskiewicz KMMarshall SWBarr WRandolph CCantu RC: Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. JAMA 290:255625632003

  • 17

    McCrea MGuskiewicz KMRandolph CBarr WBHammeke TAMarshall SW: Effects of a symptom-free waiting period on clinical outcome and risk of reinjury after sport-related concussion. Neurosurgery 65:8768832009

  • 18

    McCrea MKelly JPRandolph CCisler RBerger L: Immediate neurocognitive effects of concussion. Neurosurgery 50:103210422002

  • 19

    McCrory PMeeuwisse WJohnston KDvorak JAubry MMolloy M: Consensus statement on Concussion in Sport 3rd International Conference on Concussion in Sport held in Zurich, November 2008. Clin J Sport Med 19:1852002009

  • 20

    McKee ACCantu RCNowinski CJHedley-Whyte ETGavett BEBudson AE: Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 68:7097352009

  • 21

    Miller JRAdamson GJPink MMSweet JC: Comparison of preseason, midseason, and postseason neurocognitive scores in uninjured collegiate football players. Am J Sports Med 35:128412882007

  • 22

    Moser RSSchatz PJordan BD: Prolonged effects of concussion in high school athletes. Neurosurgery 57:3003062005

  • 23

    Putukian MAubry MMcCrory P: Return to play after sports concussion in elite and non-elite athletes?. Br J Sports Med 43:Suppl 1i28i312009

  • 24

    Randolph CMillis SBarr WBMcCrea MGuskiewicz KMHammeke TA: Concussion symptom inventory: an empirically derived scale for monitoring resolution of symptoms following sport-related concussion. Arch Clin Neuropsychol 24:2192292009

  • 25

    Schwarz A: Former Bengal Henry found to have had brain damage. New York Times June282010. (http://www.nytimes.com/2010/06/29/sports/football/29henry.html) [Accessed October 6 2010]

  • 26

    Schwarz AKlein JZ: Brain damage found in hockey player. New York Times December172009. (http://www.nytimes.com/2009/12/18/sports/hockey/18concussion.html?_r=1) [Accessed October 6 2010]

  • 27

    Shuttleworth-Edwards AB: Central or peripheral? A positional stance in reaction to the Prague statement on the role of neuropsychological assessment in sports concussion management. Arch Clin Neuropsychol 23:4794852008

  • 28

    Williamson IJSGoodman D: Converging evidence for the under-reporting of concussions in youth ice hockey. Br J Sports Med 40:1281322006

  • 29

    Zemper ED: Two-year prospective study of relative risk of a second cerebral concussion. Am J Phys Med Rehabil 82:6536592003

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Article Information

Address correspondence to: Paul Sean Echlin, M.D., 320 Adelaide Street, South London, Ontario, Canada N5Z 3L2. email: p_echlinfp@hotmail.com.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Graph demonstrating change of the SCAT2 symptom inventory total during the recovery period.

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    Graph showing SCAT2 SAC total scores for concussed athletes during the recovery period.

  • View in gallery

    Graph demonstrating changes of SCAT2 Modified BESS total scores for concussed athletes during the recovery period.

References

1

Bleiberg JCernich ANCameron KSun WPeck KEcklund PJ: Duration of cognitive impairment after sports concussion. Neurosurgery 54:107310802004

2

Broglio SPSosnoff JJFerrara MS: The relationship of athlete-reported concussion symptoms and objective measures of neurocognitive function and postural control. Clin J Sport Med 19:3373822009

3

Collins MWLovell MRIverson GLCantu RCMaroon JCField M: Cumulative effects of concussion in high school athletes. Neurosurgery 51:117511812002

4

De Beaumont LLassonde MLeclerc SThéoret H: Long-term and cumulative effects of sports concussion on motor cortex inhibition. Neurosurgery 61:3293372007

5

De Beaumont LThéoret HMongeon DMessier JLeclerc STremblay S: Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 132:6957082009

6

Echlin PSTator CHCusimano MDCantu RCTaunton JEUpshur REG: A prospective study of physician-observed concussions during junior ice hockey: implications for incidence rates. Neurosurg Focus 29:5E42010

7

Gaetz MGoodman DWeinberg H: Electrophysiological evidence for the cumulative effects of concussion. Brain Inj 14:107710882000

8

Guskiewicz KMMarshall SWBailes JMcCrea MCantu RCRandolph C: Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery 57:7197262005

9

Guskiewicz KMMarshall SWBailes JMcCrea MHarding HP JrMatthews A: Recurrent concussion and risk of depression in retired professional football players. Med Sci Sports Exerc 39:9039092007

10

Guskiewicz KMMcCrea MMarshall SWCantu RCRandolph CBarr W: Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 290:254925552003

11

Guskiewicz KMWeaver NLPadua DAGarrett WE Jr: Epidemiology of concussion in collegiate and high school football players. Am J Sports Med 28:6436502000

12

Iverson GLBrooks BLCollins MWLovell MR: Tracking neuropsychological recovery following concussion in sport. Brain Inj 20:2452522006

13

Iverson GLGaetz MLovell MRCollins MW: Cumulative effects of concussion in amateur athletes. Brain Inj 18:4334432004

14

Macciocchi SNBarth JTAlves WRimel RWJane JA: Neuropsychological functioning and recovery after mild head injury in collegiate athletes. Neurosurgery 39:5105141996

15

Makdissi MMcCrory PUgoni ADarby DBrukner P: A prospective study of postconcussive outcomes after return to play in Australian football. Am J Sports Med 37:8778832009

16

McCrea MGuskiewicz KMMarshall SWBarr WRandolph CCantu RC: Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. JAMA 290:255625632003

17

McCrea MGuskiewicz KMRandolph CBarr WBHammeke TAMarshall SW: Effects of a symptom-free waiting period on clinical outcome and risk of reinjury after sport-related concussion. Neurosurgery 65:8768832009

18

McCrea MKelly JPRandolph CCisler RBerger L: Immediate neurocognitive effects of concussion. Neurosurgery 50:103210422002

19

McCrory PMeeuwisse WJohnston KDvorak JAubry MMolloy M: Consensus statement on Concussion in Sport 3rd International Conference on Concussion in Sport held in Zurich, November 2008. Clin J Sport Med 19:1852002009

20

McKee ACCantu RCNowinski CJHedley-Whyte ETGavett BEBudson AE: Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 68:7097352009

21

Miller JRAdamson GJPink MMSweet JC: Comparison of preseason, midseason, and postseason neurocognitive scores in uninjured collegiate football players. Am J Sports Med 35:128412882007

22

Moser RSSchatz PJordan BD: Prolonged effects of concussion in high school athletes. Neurosurgery 57:3003062005

23

Putukian MAubry MMcCrory P: Return to play after sports concussion in elite and non-elite athletes?. Br J Sports Med 43:Suppl 1i28i312009

24

Randolph CMillis SBarr WBMcCrea MGuskiewicz KMHammeke TA: Concussion symptom inventory: an empirically derived scale for monitoring resolution of symptoms following sport-related concussion. Arch Clin Neuropsychol 24:2192292009

25

Schwarz A: Former Bengal Henry found to have had brain damage. New York Times June282010. (http://www.nytimes.com/2010/06/29/sports/football/29henry.html) [Accessed October 6 2010]

26

Schwarz AKlein JZ: Brain damage found in hockey player. New York Times December172009. (http://www.nytimes.com/2009/12/18/sports/hockey/18concussion.html?_r=1) [Accessed October 6 2010]

27

Shuttleworth-Edwards AB: Central or peripheral? A positional stance in reaction to the Prague statement on the role of neuropsychological assessment in sports concussion management. Arch Clin Neuropsychol 23:4794852008

28

Williamson IJSGoodman D: Converging evidence for the under-reporting of concussions in youth ice hockey. Br J Sports Med 40:1281322006

29

Zemper ED: Two-year prospective study of relative risk of a second cerebral concussion. Am J Phys Med Rehabil 82:6536592003

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