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Despite the high prevalence and potentially serious outcomes associated with concussion in athletes, there is little systematic research examining risk factors and short- and long-term outcomes. Objectives To assess the relationship between concussion history and learning disability (LD) and the association of these variables with neuropsychological performance and to evaluate post concussion recovery in a sample of college football players. Design, Setting, and Participants A total of 393 athletes from 4 university football programs across the United States received preseason baseline evaluations between May 1997 and February 1999. Subjects who had subsequent football-related acute concussions (n = 16) underwent neuropsychological comparison with matched control athletes from within the sample (n = 10). Main Outcome Measures Clinical interview, 8 neuropsychological measures, and concussion symptom scale ratings at baseline and after concussion. Results Of the 393 players, 129 (34 %) had experienced 1 previous concussion and 79 (20 %) had experienced 2 or more concussions.
Multivariate analysis of variance yielded significant main effects for both LD (P . 001) and concussion history (P = . 009), resulting in lowered baseline neuropsychological performance. A significant interaction was found between LD and history of multiple concussions and LD on 2 neuropsychological measures (Trail-Making Test, Form B [P = . 007 ] and Symbol Digit Modalities Test [P = . 009 ]), indicating poorer performance for the group with LD and multiple concussions compared with other groups. A discriminant function analysis using neuropsychological testing of athletes 24 hours after acute in-season concussion compared with controls resulted in an overall 89. 5 % correct classification rate. Conclusions Our study suggests that neuropsychological assessment is a useful indicator of cognitive functioning in athletes and that both history of multiple concussions and LD are associated with reduced cognitive performance. These variables may be detrimentally synergistic and should receive further study.
JAMA. 1999; 282: 964 - 970 The management of mild traumatic brain injury (MTBI; eg, concussion, defined as a traumatically induced alteration in mental status not necessarily resulting in loss of consciousness) in athletics is currently one of the most compelling challenges in sports medicine. Despite the high prevalence 1 and potentially serious outcomes 2, 3 associated with concussion, systematic research on this topic is lacking. Many sports medicine practitioners are not satisfied with current return-to-play and treatment options, which do not appear to be evidence based. 4 - 6 There is also little research examining whether long-term cognitive morbidity is associated with concussion. Past research with non athletes revealed that repeated concussions appear to impart cumulative damage, resulting in increasing severity and duration with a second MTBI occurring within 48 hours. 7 No data were presented which addressed more long-term outcomes.
Although survey data have shown that a prior history of head injury increases the risk for sustaining subsequent MTBI, 8 other potential risk factors associated with sports-related concussion have not been identified. Learning disability (LD), the etiology of which is presumably secondary to central nervous system dysfunction, 9 refers to a heterogeneous group of disorders manifested by difficulties in the acquisition and use of listening, speaking, writing, reading, reasoning, or mathematical abilities and which is traditionally diagnosed in early childhood. 10, 11 The incidence of diagnosed LD is 11. 8 % in the general university population. 12 However, no study to date has addressed whether LD may represent a risk factor (such as that seen with prior head injury) for poor outcome following sports-related MTBI in college athletes. Previous research has outlined the reliability, validity, and sensitivity of neuropsychological tests in assessing the specific cognitive areas associated with MTBI in the general population. 13 - 15 To date, 3 published studies have examined the use of neuropsychological testing in US football players. 16 - 18 The only multicenter study 16 was conducted in the mid- 1980 s and was designed to address the acute effects of concussion. The current study was designed to address 2 issues: first, to investigate whether a relationship exists between prior concussion and diagnosed LD among college football players and determine the influence of these variables, in isolation and combination, on baseline neuropsychological performance; and second, to evaluate the use of a neuropsychological test battery in diagnosing concussion and delineating recovery of cognitive function following MTBI in athletes. METHODS Subjects Participants in this study consisted of 393 male college football players from 4 Division IA football programs: Michigan State University, East Lansing (n = 119); the University of Florida, Gainesville (n = 106); the University of Pittsburgh, Pittsburgh, Pa (n = 85); and the University of Utah, Salt Lake City (n = 83). At the initial preseason baseline session, the following self-reported data were collected: age, playing position, SAT/ACT scores (Scholastic Aptitude Test/American College Testing, ie, college entrance examination scores), history of LD, neurological history (eg, central nervous system neoplasm or epilepsy), history of psychiatric illness (eg, depression and / or mania or anxiety), history of alcohol and / or drug abuse, prior sports played, and history of concussion.
Educational records at each institution were used to verify a documented history of diagnosed LD. A standardized concussion history form was administered at baseline to obtain detailed information regarding previous concussions, year of concussion, description of incident, nature and duration of relevant symptoms (eg, confusion and / or disorientation, retrograde and / or anterograde amnesia, and loss of consciousness), neuroimaging results (if any), and days lost from participation in football (if any). Athletes who reported amnesia were asked to provide any known collateral information from the athletic trainer, sports-medicine physician, or other source familiar with the details of the incident. All previous concussions were classified using the practice parameter of the American Academy of Neurology. 19 Protocol and Outcome Measures Preseason Baseline Evaluation Appropriate review for research with human subjects was granted separately from the 4 institutions at which the participants were enrolled. Each participant provided written informed consent for voluntary participation. All data collection was completed by the research team of clinical neuro psychologists (clinicians with PhDs or doctoral-level students) or team physicians or athletic trainers who were thoroughly trained in the use of the measures.
Each examiner was required to attend a 2 -hour workshop and was supervised during test adminstration (by M. W. C. ) to facilitate the appropriate standardized administration of the test battery. All measures were administered and scored in a standardized manner to minimize differences between test administrators and institutions. Project investigators trained in neuropsychological assessment completed all data scoring and interpretation. Baseline data collection at 3 universities (Michigan State University, University of Pittsburgh, and University of Florida) was completed prior to the 1997 / 98 and 1998 / 99 football seasons during the months of May to August.
Baseline data collection at the University of Utah occurred during February 1999 for the 1999 / 2000 season (only baseline data from the University of Utah were used for analyses). Approximately 95 % of all roster football players (scholarship and scout team players) voluntarily participated in the project. At these baseline sessions, demographic and player history information was obtained via interview. Each athlete was then administered a battery of neuropsychological tests (approximately 30 minutes in length) that is used by the National Football League. 17, 20 Tests in the battery were the Hopkins Verbal Learning Test (HVLT; verbal learning, delayed memory); Trail-Making Tests, Forms A and B (Trails A and Trails B; visual scanning and executive functioning); Digit Span Test (attention and concentration); Symbol Digit Modalities Test (SDMT; information processing speed); Grooved Pegboard Test, dominant and nondominant hand (bilateral fine motor speed); and the Controlled Oral Word Association Test (COWAT; word fluency). This test battery, described in detail elsewhere, 17 was constructed to evaluate multiple aspects of cognitive functioning.
In addition to neuropsychological testing, athletes also completed the Concussion Symptom Scale 17 to assess a baseline level of self-reported symptoms. This Likert scale consists of 20 symptoms commonly associated with concussion (eg, headache, dizziness, and trouble falling asleep), with symptoms ranging from none (score, 0) to severe (score, 6). Post concussion Evaluation Athletes who sustained a concussion during the course of a season underwent serial neuropsychological evaluations following the incident (within 24 hours of the incident, and at days 3, 5, and 7 post injury). Concussion was defined according to the American Academy of Neurology practice parameter. 19 Thus, players experiencing a traumatically induced alteration in mental status, not necessarily resulting in a loss of consciousness, were included.
Athletic trainers initially identified the majority of suspected concussions, and respective team physicians performed the examinations and made the final decisions. Once the diagnosis was established, neuropsychological testing was administered as soon as possible following injury (within 24 hours in all cases). The neuropsychological tests and self-report inventory used in the post injury phase were identical to those used at baseline, although alternate and reliable forms of the HVLT and COWAT were administered to minimize learning effects associated with these measures. Football players from within the sample served as controls. Control athletes were matched with athletes who sustained concussion according to ACT/SAT scores, history of LD, history of previous concussion, institution, and playing position. In addition, to control for exertion, each control athlete was tested within the same time frame as the athletes who experienced concussion (eg, following a game or practice).
Within the context of these variables, it was possible for controls to be matched to more than 1 player with concussion. No control athlete experienced a concussion during the course of the study. Controls were excluded from further study. Data Analysis Data from the 4 universities were pooled and analyzed using Statistica Version 5. 1 statistical software for Windows. 23 To explore the relationship between prior history of concussion, diagnosis of LD, and neuropsychological baseline performance, multiple analysis of variance (MANOVA) was performed. Concussion history (no prior concussion vs 1 vs 2 concussions) and LD (positive or negative diagnosis) were entered as independent variables, and cognitive and symptom total scores were entered as dependent measures. The MANOVA design was selected to allow an analysis of performance differences between the athletes with different concussion and LD histories, across multiple neuropsychological domains.
This design also permitted an analysis of possible interaction effects between concussion and LD histories. For in-season (post concussion) data, a discriminant function classification analysis was conducted to determine the accuracy of the neuropsychological test battery in separating athletes with concussions from control athletes within 24 hours of concussion. The 8 tests constituting the neuropsychological test battery were used as predictor variables, and membership in the group with concussions or control group was used as the dependent (grouping) variable. To provide preliminary information regarding the recovery pattern of athletes with concussions relative to the control group and to their own baseline performance, standard scores were created to convert the selected neuropsychological test scores to a common metric. These standard scores were constructed so that baseline performance for each group would have a mean of 100 and SD of 15. 21 Group differences of one-half SD (7. 5 standard score units) are considered to reflect at least a moderate difference between the means. 22 Any deviation from 100 indicates a change in performance relative to baseline for each group. The recovery pattern of players who sustained concussion across different time intervals was evaluated by standardizing all neuropsychological test results and comparing performance of the athletes with concussion with controls performance within 24 hours, and at 3, 5, and 7 days post injury.
RESULTS Demographic Data and Concussion History The multi university sample included 393 male football players with a mean (SD) age of 20. 4 (1. 7) years andean (SD) years in college. Forty-six percent of the sample was African American, 48 % European American, 4 % Polynesian American, 1 % Asian American, and 1 % Hispanic American. Of the 393 players, 6 % (n = 25) were quarterbacks; 8 % (n = 33), running backs; 13 % (n = 52), wide receivers; 16 % (n = 64), offensive linemen; 6 % (n = 23), tight ends; 17 % (n = 67), defensive backs; 16 % (n = 61), defensive linemen; 13 % (n = 48), linebackers; and 5 % (n = 20), kickers. Of the players completing the ACT examination to qualify for college admission (n = 180), the mean (SD) score was 20. 0 (1. 7). Of those qualifying with the SAT (n = 200), the mean (SD) score was 952. 9 (149. 1). College admission scores were missing for 13 individuals.
Three players in the sample reported a documented history of diagnosed psychiatric illness (eg, bipolar disorder and major depression). These players completed the baseline evaluation, but were excluded from further study. No player in the sample reported a diagnosis of major neurological disorder or history of abuse of alcohol or other drugs. Forty-six percent (n = 179) of the sample reported no prior history of concussion, 34 % (n = 129) reported experiencing 1 concussion of any grade, and 20 % (n = 79) reported a history of 2 or more sustained concussions (range, 2 - 10) of any grade. A significant relationship was found between total years participating in football and total number of concussions sustained (r = 0. 15; P. 02).
Quarterbacks (17 of 25) and tight ends (15 of 23) had the the highest rates of prior concussion (68 % and 65 %, respectively). Running backs-fullbacks (11 of 33) and kickers-punters experienced the lowest rates of prior concussion (33 % and 46 %, respectively). The prevalence of LD within the total sample of 393 athletes was 13. 5 % (n = 53). Of the players with no history of concussion (n = 179), 10. 6 % (n = 19) had a diagnosed LD; of those who had experienced 1 prior concussion (n = 129), 14. 7 % (n = 19) had diagnosed LD, and of those who had experienced multiple concussions (n = 79), 19. 0 % (n = 15) had a diagnosed LD.
Although these data suggest a possible trend between history of LD and history of multiple concussions, this relationship was not statistically significant (2 = 3. 74; P = . 15). Previous Concussions, LD History, and Baseline Neuropsychological Performance The MANOVA yielded significant main effects for both LD (F = 4. 57; P . 001) and concussion history (F = 1. 91; P = . 009) on neuropsychological test results, which indicated that both of these variables were significantly related to overall neuropsychological performance. The interaction of LD and concussion history was not significant (F = 1. 17; P = . 28). A follow-up series of univariate F tests was completed to identify the specific neuropsychological measures that accounted for the significant MANOVA. Tests for the LD main effect were Trails B (F = 15. 98; P . 001); SDMT (F = 22. 9; P . 001); COWAT (F = 11. 6; P . 001); and Hopkins delayed memory (F = 11. 8; P . 001). For the history of concussion main effect, significant tests included Trails B (F = 6. 1; P = . 002); SDMT (F = 7. 8; P . 001); and total symptoms reported (F = 4. 6; P = . 01).
To evaluate concussion group differences on the neuropsychological tests, additional post hoc analyses were conducted using the Tukey Honest Significant Difference test for unequal subjects. 24 Table 1 presents the group means (SDs) for athletes. The group with no history of concussion reported fewer symptoms than both the single concussion group (P = . 04) and the multiple concussion group (P . 001) on the concussion symptom inventory. Baseline symptoms increased as the number of concussions increased. On Trails B, the multiple concussion group performed significantly worse at baseline than the group with no history of concussion (P = . 02) and the single concussion group (P . 001). Baseline data also differed significantly on the SDMT with the multiple concussion group performing worse than both the group with no history of concussion (P = . 008) and the single concussion group (P . 001). These findings are not attributed to preexisting group differences in terms of aptitude as the multiple concussion group had higher SAT and ACT scores than did the group with no history of concussion and the single concussion group.
The table presents demographic and neuropsychological test data for the group with LD and the group without LD. To investigate the interplay between concussion history and LD on baseline neuropsychological test performance, a concussion history and LD interaction term was constructed. Univariate F tests for all 10 neuropsychological variables demonstrated statistically significant interactions for Trails B (F = 4. 99; P = . 007) and SDMT (F = 4. 74; P = . 009). In both cases, athletes with a history of multiple concussions and LD performed significantly worse than did athletes with no history of LD who had experienced multiple concussions (Figure 1). In-Season Concussions Nineteen players in the study sample were diagnosed by team medical staff as sustaining a concussion during the course of the 1997 - 1999 seasons. Thirteen individuals sustained a grade 1 concussion (mental status abnormalities resolved within 15 minutes), 4 athletes sustained a grade 2 concussion (mental status abnormalities that lasted longer than 15 minutes, but resolved within 45 minutes), and 2 athletes sustained a grade 3 concussion (brief [approximately 5 - 10 seconds] loss of consciousness).
The time between baseline testing and in-season c Michael W. Collins, PhD; Scott H. Grinder, MD; Mark R. Lovell, PhD; Duane E. Dede, PhD; David J. Moser, PhD; Benjamin R.
Pain, BS; Sally Note, MA, ATC; Michael Was, MEd, ATC; David Carry, MA; Michelle Klotz Daugherty, MA; Samuel F. Sears, PhD; Guy Nicolette, MD; Peter Indelicate, MD; Douglas B. McKeag, MD
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