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BRAIN INJURY, VOL. 18, NO.5(MAY 2004), 433–443
Cumulative effects of concussion in
amateur athletes
GRANT L. IVERSONy,MICHAEL
GAETZy,MARKR.LOVELLz and
MICHAEL W. COLLINSz
yUniversity of British Columbia, Vancouver, BC, Canada
zUniversity of Pittsburgh Medical Center, Pittsburgh, PA, USA
(Received 17 December 2003; accepted 20 June 2003)
Primary objective: To examine the possibility that athletes with multiple concussions show cumulative
effects of injury.
Methods and procedures: Amateur athletes with a history of three or more concussions were carefully
matched (gender, age, education and sport) with athletes with no prior concussions. All completed
a computerized neuropsychological test battery at preseason (ImPACT) and then within 5 days of
sustaining a concussion (mean ¼ 1.7 days).
Main outcomes and results: There were differences between groups in symptom reporting and memory
performance. At baseline (i.e. preseason), athletes with multiple concussions reported more symptoms
than athletes with no history of concussion. At approximately 2 days post-injury, athletes with multiple
concussions scored significantly lower on memory testing than athletes with a single concussion.
Athletes with multiple concussions were 7.7 times more likely to demonstrate a major drop in memory
performance than athletes with no previous concussions.
Conclusions: This study provides preliminary evidence to suggest that athletes with multiple concussions
might have cumulative effects.
Introduction
Children and adolescents frequently experience concussion in sports or other physi-
cal activities. Of particular concern is competition at the high school level, where
at least 1.25 million athletes compete in contact sports. An estimated 62 816 cases
of concussion occur annually at the high school level, with American football
accounting for about 63% of cases [1]. It is well known that many people who
sustain concussions experience post-concussion symptoms and decrements on neuro-
psychological testing during the first week post-injury [2–5]. Fortunately, the vast
majority of people who sustain a single concussion recover relatively quickly and
fully. Recovery has been demonstrated in trauma patients [5, 6], athletes [4],
children [7], and the elderly [8,9]. Although the vast majority of people who
sustain concussions eventually recover, concussions can be significant injuries that
Brain Injury ISSN 0269–9052 print/ISSN 1362–301X online # 2004 Taylor & Francis Ltd
http://www.tandf.co.uk/journals
DOI: 10.1080/02699050310001617352
Correspondence to: Grant Iverson, PhD, Department of Psychiatry, 2255 Wesbrook Mall,
University of British Columbia, Vancouver, BC, Canada V6T 2B4. e-mail: giverson@interchange.
ubc.ca.
result in distressing symptoms and clear declines in measured cognitive abilities.
Concussions should not be dismissed lightly, and young people with ongoing
symptoms (e.g. headaches or feeling ‘foggy’) should be managed conservatively.
Unfortunately, there is very little research on concussions in high school athletes.
This lack of research is alarming for several reasons. First, based on participation
levels, the largest group of at-risk athletes is at the high school level or below.
Second, at least 17 deaths related to second impact syndrome (which results from
a second concussive insult closely following the first) were reported in the literature
between 1992 and 1997 [10], and periodic cases continue to be reported. The
majority of victims have been high school athletes between the ages of 13 and
18 years, suggesting the possibility of greater vulnerability to severe injury in
children and adolescents versus adults. However, this vulnerability has yet to be
established empirically. It is important to be aware of second impact syndrome,
while keeping in mind that it is an extremely rare phenomenon. The vast majority
of amateur athletes who sustain light concussions recover quickly and fully, typically
within 3–10 days [4, 11–13].
In sport, the risk for long-term problems is rarely, if ever, associated with a single
concussion. Rather, long-term problems are believed to be associated with multiple
concussions. Awareness of the detrimental effects of repetitive concussions has
existed in modern-era sports medicine for decades both anecdotally and in the
clinical literature. Early examples from boxing include Martland’s [14] work on
dementia pugilistica (punch-drunk syndrome) and later chronic [15] and traumatic
boxer’s encephalopathy [16]. More recently, concussion in sport, and the aftermath
of multiple concussions, has been witnessed by the masses as numerous professional
athletes have had their careers prematurely ended due to these injuries.
Sports involving impact to the head such as American football, boxing and ice
hockey provide an opportunity to explore the effects of multiple concussions.
Peerless and Rewcastle [17] noted that boxers appear to make a rapid and full
recovery from a single slight concussion, but after repeated episodes, there is a
gradual appearance of permanent sequelae. The risk of sustaining a concussion in
American football has been reported to be four-to-six times greater if the player has
already sustained a concussion [18]. Permanent brain injuries due to multiple
concussions have been reported in ice hockey players [19]. In a study employing
neuropsychological testing, researchers suggested that cumulative effects of concus-
sion might be detectable in amateur soccer (i.e. Association football) players [20];
however, other researchers have reported no adverse effects associated with partic-
ipation in competitive soccer [21]. In a large study involving college American
football players, athletes with a history of two or more concussions reported
more preseason (i.e. baseline) symptoms, and they performed more poorly on
two tests designed to measure information processing speed than athletes with no
previous concussions [11]. In the most frequently cited study, Gronwall and
Wrightson [22] reported that trauma patients, some with multiple concussions,
scored significantly lower on an auditory processing task than patients with only
one concussion. In addition, a recent study demonstrated statistical differences in
post-concussion symptoms and cognitive event-related potentials at baseline for
young amateur hockey players with zero versus three or more concussions [23].
Animal models of neurotrauma suggest that limited but significant damage to
neurons can result from a single concussion (although the animal research typically
involved much more serious traumatic brain injuries than the concussions sustained
434 G. L. Iverson et al.
in sports). The notion of a continuum of injury [17, 24] implies that as acceleration/
deceleration forces increase, the number of cells damaged will increase and that
damage will progressively occur in deeper structures. Gennarelli [25] described
a continuum of injury with four stages based on increasingly severe strains on
nodal and paranodal regions of axons. Stage 2 damage (axonal ‘stretch’ from 5 to
10%) resulted primarily in transient cellular dysfunction and marked the initiation of
limited cell death.
Different types of neurons appear to be susceptible to acceleration/deceleration
forces, that are largely dependent on the amount of force and the direction of
movement of the head. In addition, neurons may be differentially susceptible to
acceleration/deceleration forces. For instance, when axons change direction to
accommodate the presence of a blood vessel, enter target nuclei (e.g. the grey/
white interface), decussate, or are of large calibre, they may be more susceptible to
injury [26–29]. Although researchers who employ animal models have demon-
strated the effects of single injuries on subsequent brain functions and structure,
little evidence is available on the effects of multiple concussions. Early studies
employing animal models designed to contrast repetitive versus single impact of
concussive and subconcussive injuries suggested that after a single subconcussive
impact, no change was observed in animal behaviour or histology. In contrast,
repetitive subconcussive episodes between 5 and 20-s intervals often resulted in
permanent injury [30, 31]. Obviously, it is very difficult to extrapolate from animal
research to concussions sustained by humans in sport. Nonetheless, a basic science
foundation for possible cumulative effects is apparent.
The purpose of this study was to replicate and extend the results of previous
studies that reported increased post-concussion symptoms at baseline for amateur
athletes who sustained multiple concussions versus those who had not sustained
a concussion. In addition, the severity of on-field markers and symptoms following
a subsequent concussion were examined to determine whether athletes with a history
of multiple concussions experience more severe symptoms and greater measured
neuropsychological decrements than athletes with no prior concussions.
Methods
Subjects
All subjects participated in the University of Pittsburgh Medical Center Sports
Concussion Program. The programme uses preseason and post-injury neuropsycho-
logical testing protocols to help determine return to play in athletes sustaining
concussions. Immediate Post Concussion Assessment and Cognitive Testing
(ImPACT), a computer-based demographic, symptom and neuropsychological
test program, was used at baseline and at each post-concussion follow-up assessment.
Amateur athletes with three or more concussions were selected from a large
database of players who took part in the programme. Only subjects with complete
data at baseline and at 1–2 day follow-up were included. A sample of 19 athletes,
11 high school and eight college, were identified. A sample of athletes who were
matched on age, education, level (high school or college), gender, sport, and days
post-injury was then carefully selected. The results of this matching are presented in
table 1. Therefore, the total sample consisted of 38 players, 19 with a history of
three or more concussions and 19 with no prior concussions. Because of the careful
Cumulative effects of concussion in amateur athletes 435
matching, there obviously were no statistically significant differences between
groups on the demographic variables.
Measures
ImPACT is a computer-administered neuropsychological test battery that consists of
seven individual test modules that measure aspects of cognitive functioning includ-
ing attention, memory, reaction time and processing speed. It also contains a post-
concussion symptom scale.
The memory index is comprised of five subtest scores measuring different aspects
of memory including verbal (word) learning and recognition memory, visual associa-
tive memory, visual working memory, and letter memory. This composite index
represents the average per cent correct score for these five scores. The test battery
is designed to minimize practise effects by randomizing the stimuli. With the excep-
tion of the recognition word memory test, presentation of all stimuli is varied auto-
matically for each examination. For example, for each administration of the symbol
match, three letter memory, and visual memory tasks (X’s and O’s), the computer
automatically randomizes the stimuli presented to minimize memorization of the
presented sequences across multiple evaluations. The word memory module has five
separate forms. To make up the five word lists, the words were randomly selected
from a group of single syllable nouns. In addition to the 12 target words, each word is
paired with a similar but not identical word (e.g. ‘snow or ice’, ‘doctor or nurse’).
Table 1. Demographic information, preseason testing, post-concussion testing, and on-field injury severity
markers by group
Variable No previous concussions Three or more concussions
Age (years) 17.9 (median ¼ 17, SD ¼ 2.7) 17.8 (17, 2.5)
Education-years 11.8 (median ¼ 11, SD ¼ 2.5) 11.9 (11, 2.5)
Gender 18 male 17 male
Education level 11 high school, 8 college 12 high school, 7 college
Sport 15 American football,
3 football, 1 baseball
14 American football, 2 football,
2 basketball, 1 lacrosse
Days post-injury 1.8 (median ¼ 1, SD ¼ 1.3) 1.6 (1, 1.5)
Number of athletes 19 19
Preseason
Subjective symptoms 5.6 (SD ¼ 8.1) 14.1 (15.8)
Reaction time 0.57 (SD ¼ 0.09) 0.55 (0.06)
Processing speed 35.7 (SD ¼ 8.1) 34.4 (10.1)
Memory 89.1 (SD ¼ 6.5) 84.7 (12.0)
Post-concussion
Subjective symptoms 21.5 (SD ¼ 23.4) 31.3 (26.4)
Reaction time 0.57 (SD ¼ 0.11) 0.56 (0.10)
Processing speed 36.6 (SD ¼ 8.0) 35.6 (7.8)
Memory 84.7 (SD ¼ 12.0) 74.5 (12.7)
On-field markers
Loss of consciousness 0 2
Retrograde amnesia 3 3
Post-traumatic amnesia 1 7
Disorientation 5 12
Five or more min of
mental status change
16
436 G. L. Iverson et al.
The module yields per cent correct recognition scores for both learning (per cent
correct recognition after two presentations) and delayed recognition (per cent correct
recognition approximately 15 min after the initial presentation).
The reaction time index represents the average time (s) to respond. All stimuli
are randomized to minimize practise effects. Three scores are used in the calculation
of the composite index. First, the distractor task for the X’s and O’s test module
(choice reaction time) requires the athlete to mouse click the left button if a blue
square appears on the screen and alternatively to right mouse click if a red circle
appears. The second score is the average correct reaction time score from the
colour-match module. For this test module, the athlete is presented with three
words (red, green, or blue) presented either in the same colour ink of the work
(e.g. the word ‘blue’ presented in blue ink) or in a different colour ink (‘red’ in
blue or green ink). Therefore, this task requires the athlete to respond rapidly while
inhibiting the impulse to respond to non-target words. Third, the average correct
reaction time score from the symbol match module consists of the average time to
respond to this task, which requires the athlete to mouse click on a given number,
when a specific symbol appears on the screen. The average correct reaction time is
divided by three to produce a score proportional to the other two scores. This final
score represents the reaction time composite index.
The visual–motor speed composite index consists of the average of two scores.
First the total number of blue squares or red circles correctly clicked during the
previously described X’s and O’s distractor task is divided by four. Second, the
distractor task from the three letters module is calculated and multiplied by three.
The three-letters module is a verbal working memory test that measures the ability
of the athlete to remember a series of three consonants that are immediately
followed by a distractor task that requires the athlete to click a randomly displayed
array of numbers in backward order from 25 to one. Therefore, the distractor task
provides a measure of visual search and visual–motor speed. The weighting of the
two scores that make up the visual processing composite index produces results in
a similar numeric range for both scores.
The post-concussion symptom scale has 21 symptoms (graded 0–6 in terms of
severity) commonly associated with concussion (e.g. headache, photosensitivity,
feeling slow, etc.). This scale was originally developed for use with the Pittsburgh
Steelers (a professional American football team) and is now used throughout profes-
sional and amateur sports [32, 33]. The athlete is asked to choose (via a mouse click)
the point on the scale that most accurately reflects his/her status with regard to each
symptom at that time.
Procedures
Athletes underwent a baseline evaluation and were administered the computerized
test battery before the 2000 and 2001 athletic seasons. ImPACT consists of a
detailed symptom and demographic questionnaire (e.g. relevant sport/medical/
concussion history information), as well as seven individual test modules that mea-
sure aspects of cognitive functioning.
A standardized concussion history questionnaire contained within the ImPACT
test battery was administered with the supervision of the test administrator. Before
athletes completing this section, test administrators communicated to them that they
were to document each prior episode of cerebral concussion that was formally
Cumulative effects of concussion in amateur athletes 437
diagnosed by a team physician or certified athletic trainer. Athletes also documented
any prior concussion that resulted in loss of playing time. Test administrators were
trained to define concussion as a ‘traumatically induced alteration in mental status
that may or may not be accompanied by a loss of consciousness’. Non sports-related
concussions were also included in the tally only if diagnosed by a physician. Based
on these criteria, athletes, under the supervision of the test administrator, entered in
the total number of concussions experienced in their history.
Administration of the computerized neuropsychological test battery was super-
vised by a team of clinical neuropsychologists, certified athletic trainers, or physi-
cians who were thoroughly trained in the administration of the measures. Given
that ImPACT is a self-administered test battery, all information is gathered in a
standardized manner.
All athletes were re-administered the computerized battery within 5 days of
injury (mean ¼ 1.7 days). In-study concussions were characterized by the on-field
presentation of one or more of the following symptoms after a blow to the head
or body: (1) any observable alteration in mental status or consciousness; (2) a con-
stellation of self-reported symptoms, such as post-traumatic headache, ‘fogginess’,
nausea/vomiting, dizziness, etc.; and/or (3) the presence of loss of consciousness,
disorientation, post-traumatic amnesia (PTA) or retrograde amnesia (RTA) as iden-
tified by on-field examination. Sports medicine practitioners present on the sideline
at the time of injury made the diagnosis of concussion.
Sports medicine practitioners carefully documented information pertaining to
markers of injury severity. On-field disorientation was assessed by questioning the
athlete’s post-injury awareness and orientation to surroundings (e.g. name the cur-
rent stadium, city, opposing team, current month/day). On-field PTA was assessed
through immediate and delayed (e.g. 0, 5, 15 min) memory for three words (e.g.
girl, dog, green). PTA was further documented at the post-injury follow-up eval-
uation by assessing the athlete’s ability to recall all information after trauma. Any
loss of memory in this latter regard indicated positive presence of PTA. On-field
retrograde amnesia was assessed by having the athlete recall events that occurring
just before their injury (e.g. events in the first quarter, memory for play preceding
trauma, score of the game). Retrograde amnesia was further documented at the
post-injury evaluation by assessing the athlete’s ability to recall information just
before trauma. Any loss of memory in this latter regard indicated positive presence
of retrograde amnesia. Loss of consciousness was documented when an athlete was
unresponsive to external stimuli as documented by on-field evaluation by team
medical personnel. By definition, athletes experiencing loss of consciousness
(LOC) also experienced a concomitant PTA. For the purposes of the present
study, athletes with any degree of LOC were categorized in the positive LOC
group rather than the PTA or retrograde amnesia group.
Results
A mixed-model 2 2 ANOVA was used to determine if there were between- and
within-group effects on each of the dependent variables (i.e. total symptoms, reac-
tion time, processing speed, and memory). For the total symptoms score, there was
a significant main effect for time; F(1, 36) ¼ 29.4, p < 0.00001, "
2
¼ 0.45. This is a
large effect size; approximately 45% of the variability in symptom scores was related
to the differences in performance across the two time intervals. There was not a
438 G. L. Iverson et al.
statistically significant group effect, although the observed power in this analysis was
very low (i.e. 0.35). In other words, there was only a 35% chance of correctly
rejecting a false null hypothesis. However, exploratory independent t-tests revealed
a significant difference between groups at preseason, with the athletes who had
multiple concussions reporting more symptoms ( p < 0.05, observed power ¼ 0.53,
d ¼ 0.71, large effect). The groups did not differ in total symptoms during the
post-injury follow-up assessment ( p ¼ 0.24; observed power ¼ 0.22, d ¼ 0.39,
small–medium effect). Again, however, low power could have affected this finding.
There was a trend toward an effect (table 1 and figure 1) and as demonstrated in the
effect size of 0.39. Specifically, the two groups differed by more than one-third of a
pooled standard deviation unit.
For the reaction time and processing speed composite scores, there were no
significant between- or within-group effects. Moreover, exploratory analyses
revealed no trends toward differences between groups.
For the memory composite score, there was a significant main effect for time;
F(1, 36) ¼ 13.1, p ¼ 0.001, "
2
¼ 0.27. This is a medium-to-large effect size; approxi-
mately 27% of the variability in memory scores was related to the differences in
performance across the two time intervals. There was also a group effect, with the
multiply concussed athletes showing greater decrements in memory functioning
than the mildly concussed subjects (F(1, 36) ¼ 7.0; p ¼ 0.012, "
2
¼ 0.16, observed
power ¼ 0.73). There was a clear trend toward lower memory performance in
the multiply concussed group at preseason ( p ¼ 0.08, two-tailed test, observed
power ¼ 0.42, d ¼ 0.59, medium effect size). These results are presented in table 1
and figure 2. If the effect size between groups remained constant and the
sample size in each group was increased from 19 to 25, then the two-tailed
p would be 0.04. The athletes with multiple concussions obtained significantly
lower memory composite scores during the post-injury assessment ( p ¼ 0.015,
observed power ¼ 0.70, d ¼ 0.83, large effect).
A 14-point drop in memory performance represents a major decline in function
between preseason and immediate follow-up (i.e. greater than 1.5 pooled SD
decline in performance). The 38 subjects were divided into two groups based
on whether they demonstrated this major decline in memory performance
0
5
10
15
20
25
30
35
Baseline 1-2 Days Post Injury
No Concussions Multiple Concussions
Figure 1. ImPACT symptom scores for the two groups.
Cumulative effects of concussion in amateur athletes 439
(i.e. 11 subjects demonstrated a major decline). A significantly greater proportion of
the athletes with multiple concussions (47.4%) versus no previous concussions
(10.5%) demonstrated a major decline in memory performance,
2
(1, 38) ¼ 6.3,
p < 0.013. The athletes with multiple concussions were 7.7 times more likely to
demonstrate a major drop in memory performance than the athletes with no
previous concussions (95% CI ¼ 1.442.7).
In terms of on-field markers, the groups did not differ in their experience of
LOC, retrograde amnesia or disorientation (table 1). Importantly, there was very low
power in all of these
2
analyses due to small sample sizes and some missing data.
There was a prominent trend toward a difference in post-traumatic amnesia
( p ¼ 0.08; odds ratio ¼ 6.4, 95% CI ¼ 0.761.2). The athletes with multiple con-
cussions were six times more likely to experience sideline-assessed post-traumatic
amnesia. Moreover, the athletes with a history of multiple concussions were signifi-
cantly more likely to evidence 5 or more min of sideline-assessed, broadly defined,
mental status disturbance ( p ¼ 0.036; odds ratio ¼ 8.3, 95% CI ¼ 0.977.6).
Discussion
The main findings of the current study were that young athletes who sustain mul-
tiple concussions reported significantly more symptoms and demonstrated a clear
trend toward lower memory scores at baseline. Given the closely matched samples,
the preseason symptom and memory findings were interpreted to be suggestive of
cumulative, lingering effects of multiple concussions. In addition, athletes with
multiple concussions showed worse on-field severity markers associated with their
next concussion as compared with athletes who were experiencing their first con-
cussion. They were six times more likely to experience post-traumatic amnesia and
approximately eight times more likely to experience 5 or more min of mental status
disturbance, broadly defined (i.e. RTA, PTA or disorientation). Finally, athletes
with multiple concussions had more adverse consequences in the acute recovery
period (i.e. 2 days) from their next concussion. That is, multiply concussed players
performed much lower on the memory testing at 2 days post-injury than the singly
concussed players. Athletes with multiple concussions were eight times more likely
65
70
75
80
85
90
Baseline 1-2 Days Post Injury
No Concussions Multiple Concussions
Figure 2. ImPACT memory composite scores for the two groups.
440 G. L. Iverson et al.
to evidence a marked drop in memory functioning from baseline to 2 days post-
injury (i.e. a 1.5 pooled SD drop in functioning). A major strength of this study was
the careful matching of athletes on important demographic variables. Major limita-
tions include the retrospective, quasi-experimental component of the study and the
small sample sizes.
The present findings are consistent with those of Gaetz et al. [23] who reported
that at baseline, subjects who sustained three or more concussions reported greater
numbers of post-concussion symptoms than those who had never sustained a con-
cussion. Variables such as headache, memory problems, and problems with ‘the
ability to think’ were more highly endorsed by those with multiple concussions.
In addition, athletes had significant increases in event-related potential latency
compared with the group with no concussions. The results are also consistent
with the findings of Collins et al. [11] in a large sample of college football players.
Those with two or more concussions reported more symptoms and performed
more poorly on two information processing speed tests than athletes with no
prior concussions.
The results of the present study have potentially important implications for the
clinical care of concussed athletes. If indeed multiple concussive injuries result in a
decline in neuropsychological performance over time, this information may be
important in helping athletes and there families make informed decisions about
the risk of continued participation in contact sports.
Not all recent studies reported evidence for cumulative effects. For example,
Macciocchi et al. reported that in matched groups of football players with either one
or two concussions, no statistical differences were observed on neuropsychological
tests such as the PASAT, Trails A and B, or the Symbol Digit Test [34]. However,
their sample sizes were very small (i.e. n ¼ 12). Perhaps there is a point where
statistical increases in symptoms occur following multiple concussions. There
might be a linear progression where cognitive problems and subjective symptoms
increase with the number of concussions sustained. Of course, severity of concus-
sion is likely as important, or even more important, than number of concussions.
Further research is required to understand these issues better.
Researchers have reported post-concussion symptoms in trauma patients who
are 1 or more years post-injury [35–37]; however, the underlying causes of these
persistent, long-term symptoms are subject to considerable debate. Moreover,
a carefully controlled, large-scale, prospective study of trauma patients with uncom-
plicated mild traumatic brain injuries demonstrated that long-term post-concussion
symptoms were rare [38]. In addition, it is well known that the so-called post-
concussion symptoms are non-specific; they occur in day-to-day life and are associ-
ated with multiple other factors and conditions such as depression, chronic pain, life
stress and personal injury litigation [39–46]. Therefore, it is possible that due to
some unknown sampling bias, the present study has inadvertently selected a group
of multiply concussed players who have increased baseline symptom reporting as
a result of other factors. Although possible, this seems unlikely. Nonetheless, repli-
cation of the current results, ideally with a larger sample, is recommended.
In conclusion, this study provides preliminary and provocative evidence to
suggest that young athletes with multiple concussions might have cumulative
effects. Specifically, these athletes are more likely to report ongoing post-concussion
symptoms, and they performed slightly worse on preseason memory testing.
Moreover, they appear to be more susceptible to sustaining injuries of greater
Cumulative effects of concussion in amateur athletes 441
severity in the future. Finally, those athletes with multiple concussions had greater
adverse consequences in the acute recovery period (i.e. 2 days) from their next
concussion.
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