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Investigating baseline neurocognitive performance
between male and female athletes with a history of
multiple concussion
Tracey Covassin,
1
Robert Elbin,
1
Anthony Kontos,
2
Elizabeth Larson
2
ABSTRACT
Objective The purpose of this study was to examine,
using a doseeresponse model, sex differences in
computerised neurocognitive performance among
athletes with a history of multiple concussions.
Design Retrospective with randomly selected
concussion cases from four levels/numbers of previous
concussion.
Setting Multicentre analysis of NCAA student-athletes.
Participants Subjects included a total of 100 male and
88 female NCAA athletes.
Intervention Sex and four mutually exclusive groups of
self-reported concussion history: (1) no history of
concussion, (2) one previous concussion, (3) two
previous concussions, (4) three or more previous
concussions.
Main outcome measurements Neurocognitive
performance as measured by a computerised
neurocognitive test battery (Immediate Postconcussion
Assessment Cognitive Testing (ImPACT)).
Results A doseeresponse gradient was found for two
or more previous concussions and decreased
neurocognitive performance. Females with a history of
two and three or more concussions performed better
than males with a history of two (p¼0.001) and three or
more concussions (p¼0.012) on verbal memory.
Females performed better than males with a history of
three or more concussions (p¼0.021) on visual memory.
Finally, there was a significant difference for sex on both
motor processing speed and reaction-time composite
scores. Specifically, males performed worse than
females on both processing speed (p¼0.029) and
reaction time (p¼0.04).
Conclusion The current study provided partial support
for a doseeresponse model of concussion and
neurocognitive performance decrements beginning at
two or more previous concussions. Sex differences
should be considered when examining the effects of
concussion history on computerised neurocognitive
performance.
Concussions remain a serious public health
concern, with approximately 1.6e3.0 million sport
concussions occurring every year in the USA.
1
Sports medicine professionals have recently pro-
moted computerised neurocognitive testing as one
objective component in a comprehensive concus-
sion management approach that can be used to
manage injured athletes.
2e5
Recent studies have
identified certain factors, such as sex and history
of concussion, which influence performance on
neurocognitive tests both before (ie, baseline) and
after a concussion (ie, prolonged recovery).
6e9
Researchers have reported sex differences in
cognitive performance at both baseline and post-
concussion.
10
Specifically, athletes with a history of
concussion demonstrated decreased neurocognitive
performance on baseline neurocognitive measures
when compared with athletes without any history
of concussion. Moreover, females took longer to
recover back to baseline neurocognitive levels
following a concussion than males. However, other
factors may play a role in these reported sex
differences. For example, the decreased neuro-
cognitive performance at both baseline and post-
injury may be a function of the actual number of
previously sustained concussions (ie, a dosee
response) rather than sex per se.
9
Surprisingly,
previous researchers have yet to explore sex differ-
ences pre- and postconcussion in neurocognitive
performance among athletes with a history of
multiple concussions.
Recent studies have documented sex differences
on neurocognitive measures commonly used for
managing concussion.
6 11 12
Barr et al
11
reported
that female high school athletes scored higher than
males on mental tracking, processing speed and
verbal initiation. Using collegiate athletes, Covassin
et al
6
reported that females performed significantly
higher on verbal memory than males, whereas
males demonstrated higher visual memory scores
than females. Brown et al
12
also reported that male
athletes performed faster on simple reaction time
and higher on matching to sample pairs than
female athletes. These researchers also reported
higher scores on the Sternberg memory search task
by females compared with males. These findings
suggest a disparity between males and females on
measures of neurocognitive performance. More
importantly, other factors such as concussion
history may interact with sex to further influence
neurocognitive performance.
A history of concussion has been found to influ-
ence the risk for subsequent concussive injury.
9 13
Specifically, the risk for future concussion ap-
pears to be higher for athletes with a history of
concussion.
913
Zemper
13
reported that athletes
with a history of concussion are 5.8 times more
likely to sustain a subsequent concussion than
athletes without a history of concussion. Guskie-
wicz et al
9
found that college athletes with
a history of three or more concussions had a higher
risk (3.4 times) of sustaining a subsequent con-
cussion than those with one (1.5 times) or two
(2.8 times) previous concussions. Guskiewicz et al
9
suggested a doseeresponse relationship between
1
Michigan State University, East
Lansing, Michigan, USA
2
Humboldt State University,
Arcata, California, USA
Correspondence to
Dr Tracey Covassin, Michigan
State University, 105 Im Sport
Circle, East Lansing, MI
48824-1049, USA;
covassin@msu.edu
Received 3 September 2009
Revised 3 September 2009
Accepted 28 October 2009
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Research paper
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the number of previously sustained concussions and the risk for
future concussion.
While there appears to be an increased risk for incident
concussion in athletes with multiple concussions, the long-term
neurocognitive effects of multiple concussions are unclear. Using
a sample of college football players, Collins et al
10
found that
athletes with a history of two or more concussions performed
worse on baseline measures of executive function and processing
speed than athletes with zero or one previous concussion.
Similarly, Moser et al
8
found that high school athletes with
a history of concussion demonstrated a similar neurocognitive
performance to athletes who had sustained a concussion within
the previous week of study, which suggests that there may be
residual effects associated with previously sustained concus-
sions. In contrast, Iverson et al
14
reported no differences between
groups of athletes with zero, one or two previous concussions on
verbal memory, visual memory, reaction time and processing
speed. More recently, Bruce and Echemendía
15
did not find any
differences on computerised or paper-and-pencil neurocognitive
test batteries between athletes with and without a history of
multiple concussions. Brown et al
12
also reported no differences
on baseline neurocognitive function in athletes with a history of
concussion.
There are mixed findings on the influence that multiple
concussions have on concussion risk and neurocognitive
outcomes. Extant literature supports a doseeresponse relation-
ship, wherein there is a linear increase in concussion risk with
each increase in previous concussions. However, few studies
support a doseeresponse relationship for number of previous
concussions and computerised neurocognitive performance.
These studies have not examined the potential interaction that
sex differences and previous concussions may have on neuro-
cognitive performance. Therefore, the purpose of this study was
to use a doseeresponse model to examine sex differences on
computerised neurocognitive performance among athletes with
a history of multiple concussions.
METHODS
Participants
Approximately 2500 collegiate and high school athletes partici-
pating in a multisite, sport-concussion surveillance project were
recruited for study. Athletes participating in baseball, softball,
football, lacrosse, volleyball, basketball, soccer, gymnastics,
rugby and wrestling were administered a baseline computerised
neurocognitive test battery. Participants who reported colour-
blindness, learning disability, attention deficit disorder/attention
deficit and hyperactivity disorder, treatment for migraines,
psychiatric disorder or substance abuse were excluded from the
current study. Athletes were also excluded from the study if they
had an invalid baseline test as indicated by the Immediate
Postconcussion Assessment Cognitive Testing (ImPACT) user
manual.
16
Approximately 2100 athletes met the inclusionary
criteria. These athletes were categorised by their self-reported
concussion history into one of four mutually exclusive groups:
(1) no history of concussion, (2) one previous concussion, (3)
two previous concussions or (4) three or more previous con-
cussions. There were 1686 athletes (males¼1170, females¼516)
with no history of concussion, 263 athletes (males¼202,
females¼61) with one previous concussion, 89 athletes (males¼66,
females¼23) with two previous concussions and 62 athletes
(males¼47, females¼15) with three or more previous concus-
sions. In order to provide for a more robust data analysis, 25
subjects were randomly selected from the overall sample for
inclusion in the study for each cell (concussion history by sex,
for a total of eight cells). However, given the low numbers of
females with a history of more than one concussion indicated
above, only 23 and 15 females were included respectively in the
two and three or more previous concussion groups.
Instrumentation
Immediate Postconcussion Assessment Cognitive Testing (ImPACT)
The ImPACT (2006) computerised neurocognitive test battery
was used to evaluate baseline neurocognitive function. This
battery comprises three general sections: (1) demographics, (2)
symptoms and (3) six neurocognitive modules. ImPACT takes
approximately 25e30 min to complete. The demographic
section includes a self-reported history of sport participation,
history of alcohol and drug use, learning disabilities, attention
deficit hyperactive disorders, major neurological disorders and
history of previous concussion. The symptom section includes
a self-reported inventory of 22 commonly reported concussion
symptoms. The neurocognitive testing section consists of six
neurocognitive modules which are compiled into four outcome
composite scores (verbal and visual memory, reaction time,
processing speed). These composite scores were the dependent
variables in this study.
The testeretest reliability for ImPACT was assessed over
8 days across four administrations, yielding correlation coeffi-
cients ranging from 0.66 to 0.85 for the verbal memory index,
0.75 to 0.88 for the processing speed and 0.62 to 0.66 for the
reaction time.
17
Using reliable change indices (RCI), repeated
administrations over a 2-week period revealed no practice
effects.
18
Schatz et al documented a combined sensitivity of
81.9% for ImPACT indices and total symptom score, and
a specificity of 89.4%; the positive likelihood ratio was approx-
imately 8:1, and the negative likelihood ratio was 2:1.
Procedures
The research protocol was approved by the University Institu-
tional Review Boards for the protection of human subjects at
each participating institution. Prior to the study, the researchers
obtained informed parental consent and assent for each minor
(ie, under 18 years), and adult consent for each adult in the
study. ImPACT testing was conducted at each participating
institution’s designated computer lab during preseason of each
sport. Athletes were administered the baseline version of
ImPACT in small groups (ie, 10 or fewer) to ensure a quiet
environment for testing. All tests were then inspected for
invalidity details according to ImPACT guidelines for scores
outside normative ranges.
16
Data analysis
ImPACTyields four clinical composite scores for verbal memory,
visual memory, processing speed and reaction time. Higher
scores on verbal and visual memory, and processing speed are
indicative of a better performance. Verbal and visual memory
scores represent the percentage correct, and processing speed is
a number composite score. Reaction time scores are presented in
seconds, with lower scores being indicative of better perfor-
mance.
A series of four 2 (sex¼male/female)34 (concussion
history¼0, 1, 2, 3+) factorial ANCOVAs (covaried for age) were
performed on verbal and visual memory, reaction time and
motor processing speed. Interactions were explored using a series
of independent t tests where appropriate. Statistical significance
for all tests was set at p¼0.05. Analyses were conducted using
the Statistical Package for the Social Sciences version 17.1.
598 J Neurol Neurosurg Psychiatry 2010;81:597e601. doi:10.1136/jnnp.2009.193797
Research paper
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RESULTS
Male and female athletes were comparable in age, height and
weight (see table 1). In addition, male and females were also
similar on concussion recency. Both male and female athletes
with a history of three or more concussions sustained their last
concussive injury 3.5363.31 and 3.5261.97 years ago, respec-
tively. Also, male and female athletes with a history of two
concussions had their last concussion 3.7162.29 and
3.6562.11 years ago, respectively, whereas male and female
athletes with one previous concussion were injured approxi-
mately 5.0264.28 and 4.7363.90 years ago, respectively. Inde-
pendent t tests were performed to determine if there were any
differences between the recency of last concussion between
males and females in each of the groups. There were no signif-
icant differences between male and females athletes with one
concussion (t
(1,48)
¼0.163, p¼0.872), two concussions
(t
(1,48)
¼0.122, p¼0.904) or three or more concussions
(t
(1,48)
¼0.007, p¼0.994). Thus, it is unlikely that recency of
concussion influenced the results of this study.
The results of a 2 (sex)34 (concussion history) ANCOVA for
verbal memory supported a significant main effects for sex
(F
(1,179)
¼22.43, p¼0.001) and history of concussion
(F
(3,179)
¼5.64, p¼0.001), and the interaction between sex and
history of concussion (F
(3,179)
¼2.67, p¼0.049). Specifically,
females performed better than males on verbal memory, and
athletes without a history of concussion performed better than
athletes with a history of two (p¼0.016) and three or more
concussions (p¼0.001: see table 2).
Post-hoc independent samples t tests revealed that females
with a history of three or more concussions performed better
than males with a history of three or more concussions
(t
(3,38)
¼2.71, p¼0.012) on verbal memory. Females with
a history of two or more concussions also performed better than
males with a history of two or more concussions (t
(3,46)
¼4.59,
p¼0.001) on verbal memory. There were no other significant
differences for verbal memory among the history of concussion
groups.
The results for visual memory supported significant differ-
ences for sex (F
(1,179)
¼4.21, p¼0.042) and history of concussion
(F
(3,179)
¼2.96, p¼0.034). Specifically, females performed better
than males on visual memory, and athletes with a history of
three or more concussions performed worse than athletes
without a history of concussion (p¼0.021). The interaction
between sex and history of concussion was not supported
(F
(3,179)
¼0.50, p¼0.68).
Finally, the results supported significant differences for sex on
both motor processing speed (F
(1,179)
¼4.85, p¼0.03) and reaction
time (F
(1,179)
¼4.26, p¼0.04). Specifically, males performed worse
than females on both processing speed and reaction time. How-
ever, the analyses revealed no significant main effect in motor
processing (F
(1,179)
¼0.7244, p¼0.54) speed and reaction time
(F
(1,179)
¼0.04, p¼0.99) among the history of concussion groups
or interaction between history of concussion and sex (motor
processing¼F
(1,179)
¼0.89, p¼0.45; reaction time¼F
(1,179)
¼0.46,
p¼0.71).
DISCUSSION
The purpose of the current study was to examine neurocognitive
performance between male and female athletes with a history of
multiple concussions. A secondary purpose was to reaffirm the
doseeresponse gradient between concussion history and
neurocognitive performance tentatively supported in the litera-
ture.
8
The results indicated that males with a history of three or
more concussions performed worse than females with a history
of three or more concussions on verbal memory. In addition,
a doseeresponse gradient for history of concussion beginning
with at least two or more previous concussions was partially
supported by this study. Athletes with no history of concussion
performed significantly better than athletes with a history of
two and three or more concussions on verbal memory.
Furthermore, athletes with a history of three or more concus-
sions performed worse than athletes without a history of
concussion on visual memory.
Athletes in this study demonstrated a doseeresponse gradient
relationship between the number of previous concussions and
cognitive performance. Specifically, athletes with a history of
two and three or more concussions performed worse than
athletes with no previous concussion on verbal memory. In
addition, athletes with a history of three or more concussions
scored worse on visual memory compared with athletes without
a history of concussion. These results are consistent with Collins
et al,
10
who found that athletes with two or more concussions
performed significantly worse than athletes with one or no
previous concussions on Trail-Making Test B and the Symbol
Digit Modalities Test. These findings suggest that a history of
a single concussion does not appear to result in long-term
neurocognitive impairments as evidenced by computerised
neurocognitive testing. However, a history of two or more
concussions may be associated with long-term deficits in exec-
utive function
10
and verbal and visual memory. The notion that
two or more previous concussions represent the threshold of
a doseeresponse gradient for the relationship between previous
concussion and neurocognitive performance is contrary to
reports that three or more concussions were necessary for any
long-term neurocognitive or other decrements.
19
The doseeresponse observed in the current study may have
been more evident for males with three or more concussions
compared with females with three or more concussions due to
males’possible under-reporting their previous concussions.
Studies suggest that male football players
20
under-report
concussions due to fear of being withheld from competition, not
realising the injury was serious enough to warrant medical
attention, and lack of awareness of concussions. As a result, the
male athletes in our study with three or more concussions may
in fact have had numerous concussions but did not report them
to a medical professional. In addition to under-reporting
concussions, male athletes may have incurred more severe
concussions in this study compared with female athletes. This
increased severity threshold could be related to that fact that
males in the current study over-represented collision sports such
as football and hockey, which generate high-velocity impacts.
Males are also socialised to play through pain and minimise
symptoms.
21
Consequently, males in the current study may
have continued to participate with a mild concussion, thus
exacerbating their injury and its effects. Unfortunately, the
current study was unable to determine the severity of concus-
sion as concussions were self-reported.
One explanation for the sex-based differences on history of
concussion in our study may be oestrogen and progesterone
Table 1 Demographic information for male and female athletes
Males (n[100) Females (n[88)
MSDMSD
Weight (kg) 84.25 26.16 62.67 8.70
Height (inches) 69.48 10.73 65.08 2.73
Age (years) 18.35 2.77 18.29 2.24
J Neurol Neurosurg Psychiatry 2010;81:597e601. doi:10.1136/jnnp.2009.193797 599
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acting as a neuroprotective factor for females following
a concussion.
22e25
Oestrogen may increase the response to
excitatory amino acids by acting directly on the glutamate
NMDA receptor,
25
which has a role in the neurometabolic
cascade following concussion.
26
However, oestrogen may also
protect neurons from excitatotoxic damage caused by ischaemia,
which may mitigate cognitive impairments.
24 27
Furthermore,
progesterone has been shown to bind to neuronal receptors
(sigma receptor, GABAa), reduce cerebral oedema and down-
regulate the inflammatory cascade in response to neurotrauma
in animals.
23
Sex differences were also observed in reaction time and motor
processing speed, with females performing better than males on
both these tasks. These results are in contrast to those of Brown
et al,
12
who found a faster reaction time for male athletes than
females on a computerised neurocognitive test (Automated
Neuropsychological Assessment Metrics: ANAM). A possible
explanation for this discrepancy may be that the ImPACT
composite score for reaction time encompasses both choice and
simple reaction time, while ANAM only includes a simple
reaction time. Our results were similar to other researchers who
reported that females performed better than males on processing
speed.
28e30
Specifically, Barr
11
reported that female high school
athletes demonstrated higher processing speed scores than male
high school athletes.
There were several limitations in this study that must be
considered when interpreting the results. History of concussion
was self-reported and therefore was susceptible to recall, recency
and other self-report effects. As a result, athletes may have
under- or over-reported their concussion history. Another limi-
tation of this study was the low representation of female
athletes in the two and three or more history of concussion
groups. Consequently, the generalisability of the current findings
to female athletes in the higher concussion history groups is
limited. Finally, the varying age (ie, college vs high school) of
subjects was a potential confounding variable in this study.
However, the confounding effects of age were statistically
accounted for using the ANCOVA analysis.
The current study is the first to explore sex differences in
athletes with and without a history of concussion using
a concussion history doseeresponse gradient. Male athletes with
a history of three or more concussions reported lower verbal
memory scores compared with female athletes with a history of
three or more concussions. As a result, clinicians may consider
managing male and female athletes differently after multiple
concussions. Also, a doseeresponse gradient was found for
athletes with a history of two and three or more concussions
compared with athletes with no previous concussions. Future
research should focus on sex and age differences in high school
and collegiate athletes with and without a history of concus-
sion. Further research is also warranted on sex differences and
recovery rates in athletes with a history of multiple concussions.
Finally, researchers should explore factors such as hormone
levels, injury severity and the accuracy of concussion history
reporting to better understand the sex differences reported in the
current study
Competing interests None.
Patient consent Obtained.
Ethics approval Ethics approval was provided by the Michigan state University and
Humboldt State University.
Contributors All authors have contributed to the three primary areas listed.
Provenance and peer review Not commissioned; externally peer reviewed.
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Table 2 Means and standard deviations for Immediate Post-concussion Assessment Cognitive Testing
composite scores by sex
Sex N
History of
concussion
Verbal memory
(mean±SD)
Visual memory
(mean±SD)
Motor processing speed
(mean±SD)
Reaction time
(mean±SD)
Males 25 0 0.90160.069 0.82060.114 39.6967.79 0.55960.077
25 1 0.88560.069 0.76960.103 40.0066.76 0.54860.068
25 2 0.82860.069 0.77460.085 37.8964.26 0.55360.076
25 3+ 0.81760.069 0.73260.081 41.6966.70 0.55960.073
Total 100 0.85860.079 0.77460.100 39.8266.55 0.55560.073
Females 25 0 0.93160.070 0.82160.106 41.1368.39 0.52860.061
25 1 0.89960.076 0.80560.082 41.2165.67 0.54160.064
23 2 0.91360.060 0.81160.108 42.7966.11 0.53960.055
15 3+ 0.89460.0949 0.77260.093 43.1964.44 0.52460.054
Total 88 0.99160.074 0.80660.098 40.81266.58 0.54560.067
600 J Neurol Neurosurg Psychiatry 2010;81:597e601. doi:10.1136/jnnp.2009.193797
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doi: 10.1136/jnnp.2009.193797
2010 81: 597-601J Neurol Neurosurg Psychiatry
Tracey Covassin, Robert Elbin, Anthony Kontos, et al.
concussion
athletes with a history of multiple
performance between male and female
Investigating baseline neurocognitive
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