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
postconcussion 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 prevalence1
and potentially serious outcomes2, 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
nonathletes 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 study16 was conducted in the mid-1980s 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 neuropsychologists (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
Scale17 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). Postconcussion 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 postinjury). 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 postinjury 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 (postconcussion) 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 postinjury.
RESULTS Demographic Data and Concussion History The multiuniversity sample
included 393 male football players with a mean (SD) age of 20.4 (1.7) years and
2.6 (1.3) mean (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

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