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Neuropsychological Impairment in Amateur Soccer Players
Erik J. T. Matser, MSc;
Alphons G. Kessels, MD;
Muriel D. Lezak, PhD;
Barry D. Jordan, MD;
Jaap Troost, MD
JAMA. 1999;282:971-973.
ABSTRACT
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Context Soccer players incur concussions during matches and training sessions, as well as numerous subconcussive blows to the head from impacts with the soccer ball (headers). The combination of soccer-related concussions and the number of headers may be a risk for chronic traumatic brain injury (CTBI).
Objective To determine whether amateur soccer players have evidence of CTBI.
Design, Setting, and Participants Cross-sectional study of 33 amateur soccer players and 27 amateur athletes involved in swimming and track (controls) in the Netherlands who underwent interviews and neuropsychological testing.
Main Outcome Measures Performance of soccer players vs controls on 16 neuropsychological tests having 27 outcomes.
Results Compared with control athletes, amateur soccer players exhibited impaired performance on tests of planning (39% vs 13%; P=.001) and memory (27% vs 7%; P=.004). Among soccer players, 9 (27%) had incurred 1 soccer-related concussion and 7 (23%) had had 2 to 5 concussions during their career. The number of concussions incurred in soccer was inversely related to the neuropsychological performance on 6 of the neuropsychological tests.
Conclusions Our results indicate that participation in amateur soccer in general and concussion specifically is associated with impaired performance in memory and planning functions. Due to the worldwide popularity of soccer, these observations may have important public health implications.
INTRODUCTION
Chronic traumatic brain injury (CTBI) is the cumulative long-term neurologic consequence of repetitive concussive and subconcussive blows to the head, and has been described primarily among professional boxers.1-4 Evidence suggests that CTBI also may be associated with professional soccer.5-6 Neuropsychological impairment and neurological abnormalities have been observed in retired amateur and active professional soccer players.7-11 A survey of active soccer players reported that neurological symptoms correlated with reported history of acute head injury received during play.12 To date, only 1 preliminary investigation evaluated neuropsychological functioning in nonprofessional high school soccer players.13 The current investigation was undertaken to determine if neuropsychological dysfunction occurs in amateur soccer players.
METHODS
Between September 1997 and May 1998, athletes from 3 complete teams of 3 different regional-league amateur soccer clubs (n=33) were compared with 27 control athletes. The control athletes were middle-distance runners (2 complete premier-league track teams) and middle-distance swimmers (1 complete premier-league team) from the same region as the soccer clubs. All participants completed an interview that inquired about age, education, lifetime number of general anesthesias, occupational history, learning disorders, lifetime number of concussions (sports- and nonsports-related), alcohol intake, drug use, and medical conditions that might affect cognitive functioning. The primary physicians for all participants were interviewed regarding the number of concussions the athletes had incurred and medical conditions that might interfere with cognitive functioning. All participants in this study were native to the Netherlands and educated in the Dutch educational system. Athletes also were excluded for history of drug use, learning disorders, epilepsy, and other medical conditions that might affect cognitive functioning. Education was scored on a 7-point scale and because all participants completed their secondary school education, only level 3 (technical and vocational training for ages 12-16 years) to level 7 (academic) were used. This study was approved by the St Anna Hospital Medical Ethical Committee and oral informed consent was obtained from all participants.
Each participant was interviewed by a neuropsychologist and received neuropsychological tests administered by an experienced psychometrician. All tests were administered according to standardized procedures. The test data were scored by a neuropsychologist who was blinded to the status of the participants. The neuropsychological tests included the Raven Progressive Matrices,14 Wisconsin Card Sorting Task,15 Paced Auditory Serial Addition Task,16 Digit Symbol Modalities Test,17 Trail-Making tests A and B,18 Stroop Test,19 Bourdon-Wiersma Test,20 Wechsler Memory Scale (Associate Learning, Logical Memory, and Visual Reproduction subtests),21 Complex Figure Test,22 15-Word Learning Test,23 Benton Facial Recognition Test,24 Figure Detection Test,25 Verbal Fluency Test,25 and Puncture Test.26
The means of the neuropsychological test scores were compared using the t test, with 1-tailed P values. The differences, their confidence intervals, and 1-tailed P values were determined with a linear regression analysis adjusting for level of education, alcohol intake, number of general anesthesias, and number of concussions not due to soccer play.
Multiple end point testing was controlled for by clustering the 27 test scores into 8 cognitive functions as described by Lezak.27 For each cluster, a global null hypothesis stating that all differences of the included test scores are 0 was tested using the ordinary least squares (OLS) test.28 For the 8 resulting 1-tailed P values, a Bonferroni correction for the significance level was applied. In addition, the means of the neurocognitive test scores among the soccer players were analyzed. Soccer players with and without soccer-related concussions were compared using the t test.
RESULTS
Soccer players were similar to controls in age, education level, nonsoccer-related concussions, and number of times they had received general anesthesia (Table 1). The soccer players exhibited a higher frequency of alcohol intake per month compared with controls.
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Table 1. Characteristics of Soccer Players and Controls
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The average duration of an amateur career was 17 years. Thirty-three percent played 5 to 15 years and 67% played more than 16 years. The average time spent in training practices was 3.6 h/wk and the median of the number of matches played annually was 36 (range, 20-70). The median number of balls headed in a match was 8.5 (range, 0-20). Nine players (27%) incurred 1 soccer-related concussion; 7 players (23%) reported 2 to 5 concussions in a career.
Amateur soccer players exhibited impairment in planning (OLS P=.001) and memory (OLS P=.004) (Table 2). These scores remained statistically significant after Bonferroni correction. After adjusting for concussions unrelated to soccer, alcohol intake, level of education, and number of general anesthesias, soccer players performed significantly poorer (1-tailed P<.05) on the Complex Figure Test (Immediate Recall [P=.03]); Digit Span Test (Forward [P=.01] and Backward [P=.01]); and Logical Memory (P=.01), Visual Reproduction (P=.04), and Associate Learning (P=.03) subtests of the Wechsler Memory Scale.
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Table 2. Psychometric Performance of Controls and Amateur Soccer Players*
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Concussions incurred in soccer were inversely correlated with performances on the Digit Span Test (Forward) (P=.004), Facial Recognition Task (P=.001), Complex Figure Test (Immediate Recall) (P=.04), Complex Figure Test (Delayed Recall) (P=.03), Digit Symbol Modalities Test (P=.03), and Logical Memory subtest of the Wechsler Memory Scale (P=.006).
COMMENT
These findings suggest that participation in amateur soccer may be associated with mild CTBI, as evidenced by impairment in cognitive functioning based on tests of memory and planning. Concussions incurred in amateur soccer may play a fundamental role in the development of cognitive impairment observed in these players.
As reported in our previous study of professional soccer players,11 amateur soccer appears to be associated with impairments in planning and memory functions. The Complex Figure Test Immediate Recall (memory) and the Wisconsin Card Sorting Task (planning) were sensitive in detecting symptoms of neurocognitive impairment in amateur soccer players. According to standards used in clinical practice,27 7% of controls and 27% of amateur soccer players showed moderately to severely impaired scores on the memory test and 13% of controls and 39% of amateur soccer players showed moderately to severely impaired scores on the planning test. The neurological effects of amateur soccer appear to be related to soccer-related concussions caused by contact trauma. Most of the memory tests that showed a significant difference between the soccer players and the controls were inversely related with concussions incurred in soccer in the intragroup analysis.
In conclusion, participation in amateur soccer is associated with decreased performance on tests of memory and planning. Although cognitive impairment appears to be mild, it presents a medical and public health concern, with 200 million Federation International Football Association–registered soccer players worldwide. Methods for surveillance and prevention should be developed and adopted to maximize safety.
AUTHOR INFORMATION
Corresponding Author and Reprints: Erik J. T. Matser, MSc, Department of Neuropsychology and Sports Neurology, St Anna Hospital, PO Box 90, 5560 AB Geldrop, the Netherlands (e-mail: akes{at}aozg.azm.nl).
Author Affiliations: Department of Neuropsychology and Sports Neurology, St Anna Hospital, Geldrop, the Netherlands (Dr Matser); Department of Anatomy, Faculty of Medicine and Health Sciences, Erasmus University, Rotterdam, the Netherlands (Dr Matser); Research Unit Patient Care (Dr Kessels) and Department of Neurology (Dr Troost), University Hospital of Maastricht, Maastricht, the Netherlands; Department of Neurology, Oregon Health Sciences University, Portland (Dr Lezak); and Traumatic Brain Injury Program, Burke Rehabilitation Hospital, White Plains, NY (Dr Jordan).
REFERENCES
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1. Critchley M. Medical aspects of boxing, particularly from a neurological standpoint. BMJ. 1957;1:357-362.
PUBMED
2. Robberts AH. Brain Damage in Boxers. London, England: Pittman Medical & Scientific Publishers Co Ltd; 1969.
3. Jordan BD. Neurologic aspects of boxing. Arch Neurol. 1987;44:453-459.
ABSTRACT
4. Mendez MF. The neuropsychiatric aspects of boxing. Int J Psychiatry Med. 1995;25:249-262.
PUBMED
5. Matser JT. Sponzen en aspirines, voldoende bij hoofdletsels in sport? Geneeskunde Sport. 1996;29:66-73.
6. Corsellis JA. Brain damage in sport. Lancet. 1976;1:401-402.
PUBMED
7. Tysvaer AT, Lochen EA. Soccer injuries to the brain. Am J Sports Med. 1991;19:56-60.
FREE FULL TEXT
8. Sortland O, Tysvaer AT. Brain damage in former association football players: an evaluation by cerebral computed tomography. Neuroradiology. 1989;31:44-48.
ISI
| PUBMED
9. Tysvaer AT, Storli O, Bachen NI. Soccer injuries to the brain. Acta Neurol Scand. 1989;80:151-156.
ISI
| PUBMED
10. Tysvaer AT, Storli O. Association football injuries to the brain. Br J Sports Med. 1981;15:163-166.
FREE FULL TEXT
11. Matser JT, Kessels AGH, Jordan BD, Lezak MD, Troost J. Chronic traumatic brain injury in professional soccer players. Neurology. 1998;51:791-796.
FREE FULL TEXT
12. Jordan SE, Green GA, Galanty H, et al. Acute and chronic brain injury in United States national team soccer players. Am J Sports Med. 1996;24:205-210.
FREE FULL TEXT
13. Witol A, Webbe F. Neuropsychological deficits associated with soccer play. Arch Clin Neuropsychol. 1994;9:104.
14. Raven JC. Guide to the Standard Progressive Matrices. London, England: HK Lewis; 1960.
15. Berg EA. A simple objective treatment for measuring flexibility in thinking. J Gen Psychol. 1948;39:15-22.
PUBMED
16. Gronwall DMA. Paced Auditory Serial Addition Task. Percept Mot Skills. 1977;44:367-373.
ISI
| PUBMED
17. Wechsler D. WAIS-R Manual. New York, NY: Psychological Corp; 1981.
18. Army Individual Test Battery: Manual of Directions and Scoring. Washington, DC: War Department Adjutant General's Office; 1944.
19. Golden CJ. Stroop Color and Word Test. Chicago, Ill: Stoelling; 1978.
20. van de Loo L. Enkele beschouwingen over de Bourdon-Wiersma test. Tijdschr Psychol Kring Nijmeegse Universiteit. 1956;2:33-46.
21. Wechsler D. Wechsler Memory Scale Manual. San Antonio, Tex: Psychological Corp; 1974.
22. Osterieth PA. Le test de copie d'une figure complexe. Arch Psychol. 1944;30:206-356.
23. Deelman BG, Brouwer WH, van Zomeren AH, et al. Functiestoornissen na trauma capitis. In: Jennekens-Schinkel A. Neuropsychologie in Nederland. Deventer, the Netherlands: Van Loghum Slaterus; 1980.
24. Benton AL, Hamsher K, Varny NR, Spreen O. Contributions to neuropsychological assessment. New York, NY: Oxford University Press; 1983.
25. Luteyn F. Een nieuwe verkorte GIT. Dutch J Psychol. 1966;2:675-682.
26. van der Vlugt H. Lateralisaties van Hersenfuncties: een Neuropsychologisch Onderzoek Naar de Relatie Tussen Handvoorkeur en de Relatie van de Taalfunctie [dissertation]. Tilburg, the Netherlands: Tilburg University; 1979.
27. Lezak MD. Neuropsychological Assessment. 3rd ed. New York, NY: Oxford University Press; 1995.
28. O'Brien PC. Procedures for comparing samples with multiple endpoints. Biometrics. 1984;40:1079-1087.
FULL TEXT
|
ISI
| PUBMED
29. Läuter J. Exact T and F tests for analyzing studies with multiple endpoints. Biometrics. 1996;52:964-970.
FULL TEXT
|
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