J Neurosurg Pediatrics 13:72–81, 2014
©AANS, 2014
Effect of sex on symptoms and return to baseline in
sport-related concussion
Clinical article
Scott L. Zuckerman, M.D.,1 Rachel P. Apple, M.D., 2 Mitchell J. Odom, B.S., 3
Young M. Lee, B.S.P.H., 3 Gary S. Solomon, Ph.D.,1 and Allen K. Sills, M.D.1
Department of Neurological Surgery, Vanderbilt Sports Concussion Center; 2Department of Medicine and
Pediatrics, Vanderbilt University School of Medicine; and 3Vanderbilt University School of Medicine,
Nashville, Tennessee
1
Object. Sport-related concussions (SRCs) among youth athletes represent a significant public health concern.
Prior research suggests that females fare worse symptomatically after an SRC. The authors aimed to assess sex differences in number, severity, and resolution of postconcussive symptoms using reliable change index (RCI) methodology applied to days to return to symptom baseline.
Methods. Between 2009 and 2011, 740 youth athletes completed valid neurocognitive and symptom testing
before and after an SRC using Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT). A total of
122 female and 122 male athletes were matched on number of prior concussions, age, and number of days to first
postconcussion test. At baseline and postconcussion, the authors compared each of the individual 22 symptoms on
ImPACT to calculate individual symptom severity and aggregate symptom severity, or the Total Symptom Score
(TSS). When comparing individual symptoms, the significance level for the comparison of each symptom was set
at 0.05/22 = 0.0023. When comparing aggregate symptom severity, or TSS, a single value was compared, requiring
an alpha set to 0.05. The number of days to return to baseline TSS was compared using RCI methods set at the 80%
confidence interval, equal to a raw score point value of 9.18 on the TSS.
Results. At baseline, females reported a greater severity for the symptom, “sleeping less than usual,” compared
with males (0.88 ± 1.49 vs 0.31 ± 0.86, p < 0.001). However, no other individual symptom severity differences were
noted before or after SRC. At baseline, females exhibited a statistically significant greater aggregate symptom severity than males (7.24 ± 10.22 vs 4.10 ± 6.52, p = 0.005). Greater aggregate symptom severity for females was also
found postconcussion (21.38 ± 19.02 vs 16.80 ± 17.07, p = 0.049). Females took longer to return to baseline TSS (9.1
± 7.1 days vs 7.0 ± 5.1 days, p = 0.013).
Conclusions. The results of this retrospective study indicate that females endorse a greater severity of symptoms
at baseline and postconcussion than males without significantly different symptom profiles. Furthermore, after suffering an SRC, females take longer to return to their baseline symptom level.
(http://thejns.org/doi/abs/10.3171/2013.9.PEDS13257)
Key Words • concussion • sports • sex • mild traumatic brain injury • symptoms • return to baseline • trauma
E
year approximately 1.7–3.8 million traumatic
brain injuries occur in the US, more than 300,000
of which are due to sports and recreational activities.21,27 Sport-related concussions (SRCs) comprise
nearly 9% of all athletic injuries and represent a major
public health concern affecting athletes of all ages.23 In
the wake of Title IX, women’s involvement in organized
sports has grown exponentially since the early 1970s
very
Abbreviations used in this paper: CISG = Concussion in Sport
Group; ImPACT = Immediate Post-Concussion Assessment and
Cognitive Testing; RCI = reliable change index; SRC = sport-related
concussion; TSS = Total Symptom Score.
72
(http://www.nfhs.org/Participation/HistoricalSearch.
aspx).36 The role of sex in SRCs has emerged as a crucial
area of study. Several studies have indicated sex differences with respect to SRC incidence,16,23,25,31,37 symptom
endorsement,4,12–14,20,30,38,39 and neurocognitive test performance,4,12,14 both in the baseline4,6,15,43 and acute, postconcussion phases.4,12,14
Although more males participate in athletics overall,
in sports governed by the same rules for both sexes, the
incidence of concussion has been shown to be higher for
female athletes than male athletes.16,23,25,31,37 At the high
school level, Lincoln et al.31 found that when similar
boys’ and girls’ sports were compared, girls’ sports had
J Neurosurg: Pediatrics / Volume 13 / January 2014
Sex and sport concussion symptoms
approximately twice the concussion risk. Moreover, the
concussion incidence rate in girls’ soccer (0.35/1000) and
girls’ lacrosse (0.30/1000), ranked second and fourth, respectively, among 12 sports, with boys’ football ranking
first (0.60/1000). Ten years prior, at the high school level,
Powell and Barber-Foss37 observed that female athletes
participating in soccer, basketball, and softball had higher
concussion rates than males participating in the equivalent sports. At the collegiate level, Hootman et al.25 found
that females had a higher concussion rate than males in
the sports of ice hockey, soccer, and basketball. After reviewing 13,591 collegiate injuries, Covassin et al.16 found
that female athletes were at higher risk for in-game concussions than males while playing soccer and basketball.
Symptoms experienced post-SRC, such as headache,
dizziness, fatigue, irritability, decreased concentration,
and memory problems, can significantly impact an athlete’s functioning. Symptom resolution is often the final factor taken into account when returning an athlete
to play.5 Although most postconcussive symptoms are
transient, a minority of athletes suffers from long-term
sequelae, lasting up to 12 months postinjury.2,9,19 A protracted recovery, often termed postconcussion syndrome,
can result in an athlete’s removal from a sport or team,
which may lead to reactive depression, interference with
both school and extracurricular activities, and participation in potentially dangerous activities, such as drugs or
alcohol.8,40 Available data suggest that male and female
athletes differ in terms of quantity and nature of symptoms following SRC, whereby females experience more
somatic symptoms, dealing with cognitive function, emotions, and sleep, than males.4,12,14,20,30,38,39
In the acute postconcussive state, females have been
shown to report increased symptoms compared with their
male counterparts.4,12,14,20,30,38,39 Frommer et al.22 evaluated
812 high school SRCs, in 610 males and 202 females, and
found that males endorsed more amnesia and confusion,
whereas females reported more drowsiness and noise sensitivity. Covassin et al.15 tested 1209 college athletes and
found small but significant sex differences in baseline
mean scores with females reporting more symptoms than
males, specifically headache, nausea, fatigue, sleeping
more than usual, drowsiness, sensitivity to light and noise,
sadness, nervousness, feeling more emotional, difficulty
concentrating, visual problems, and total symptoms.
However, this study did not control for concussion history.
Colvin et al.12 and Broshek et al.4 tested high school and
collegiate male and female athletes in the acute postconcussive state, and in both cohorts women reported more
symptoms than men. These two studies have important
methodological differences. Colvin et al.12 matched participants based on concussion history, whereas Broshek et
al.4 controlled for age, ethnicity, and helmet use, but not
concussion history. Preiss-Farzanegan et al.38 assessed
260 adult and pediatric athletes who presented to the
emergency department after sustaining an SRC and found
that females reported higher rates of headache, dizziness,
fatigue, and concentration problems than males. Furthermore, Covassin et al.14 evaluated 41 collegiate male and
38 collegiate female athletes and found that men reported
postconcussion vomiting and sadness more often than
J Neurosurg: Pediatrics / Volume 13 / January 2014
women. The authors did not control for concussion history, although multivariate analysis of variance revealed
no differences on the basis of concussion history.
In terms of time to symptom resolution, few studies
have delineated a clear difference between male and female athletes with regard to symptom duration. A study
by Colvin et al.12 found that female soccer players experienced longer-lasting headaches postconcussion than
concussed male soccer players. However, that study did
not assess time to headache resolution. In a retrospective
analysis of moderate concussions sustained by male and
female athletes ranging in age from 10 to 62 years, Cantu
et al.7 did not find any significant differences in return to
symptom baseline on the basis of sex but did find a difference on the basis of age, with athletes younger than
18 years taking longer to reach symptom resolution than
athletes older than 18 years. Most recently, Covassin et
al.13 studied high school and collegiate athletes after an
SRC and found that female athletes reported more symptoms than male athletes on Days 2, 7, and 14 postconcussion. The authors did not report data regarding time
to symptom resolution. Lastly, the previously mentioned
study by Frommer et al.22 discerned no difference in time
to symptom resolution and return-to-play between males
and females. No previous studies have found differences
based on sex and return to symptom baseline.
As further indication of the ongoing debate surrounding the role of sex in SRCs, at its fourth meeting
in 2012, the international group of experts composing
the Concussion in Sport Group (CISG) delineated several “modifying” factors that influence management of
concussions and prolonged symptoms, such as number
of previous concussions, prolonged loss of consciousness,
age, and medications.35 However, despite considerable
deliberation, the international group concluded, “There
was not unanimous agreement that the current published
research evidence is conclusive enough for [gender] to be
included as a modifying factor, although it was accepted
that gender may be a risk factor for injury and/or influence of injury severity.”35 Moreover, it is imperative to
note in any discussion of SRC that diagnosis relies heavily on self-reported symptom endorsement. In this regard,
females have been shown to be more honest and to volunteer information on postconcussive symptoms more
readily than their male counterparts.7 It remains unclear
whether concussion incidence data and symptom severity
differences represent a true disparity or are a product of
reporting bias.13–15,17,24
In an attempt to address this issue empirically, we endeavored to assess for sex differences in baseline and postconcussive symptoms, as well as time to return to symptom
baseline after SRC in a matched cohort of male and female
athletes. We also attempted to delineate the symptom variable more precisely, by using individual symptom severity
and aggregate symptom severity. Based on prior literature,
we hypothesized that female athletes, when compared with
male athletes, would 1) endorse a greater number of symptoms at baseline and postconcussion, 2) endorse a greater
symptom severity at baseline and postconcussion, and 3)
experience a longer time to return to symptom baseline as
measured by reliable change methodology.
73
S. L. Zuckerman et al.
Methods
Study Design
Institutional review board approval was obtained prior to data collection. The study design was retrospective
and observational. All participants were recruited from
middle school, high school, and college athletic programs
in the Western Pennsylvania area from 2009 to 2011 as
part of a regional neurocognitive testing program. Written informed consent was obtained from athletes age 18
years or older, and for those younger than 18 years, from
a parent or guardian.
Selection of Participants
After injury, diagnosis of concussion was made based
on the following on-field or sideline signs or symptoms: 1)
lethargy, fogginess, headache, and so on; 2) alteration in
mental status; 3) loss of consciousness; or 4) amnesia. The
diagnosis of concussion was made by an athletic trainer
or team physician. Following the recommendations of the
CISG consensus guidelines, no grading system was used
for concussion severity.34
The inclusion criteria for this study were as follows:
1) concussion sustained while playing a sport; 2) valid
completion of up to 2 postconcussion ImPACT (including
TSS) tests; 3) middle school, high school, or collegiate
athlete; and 4) English as a primary language. Exclusion
criteria were as follows: 1) invalid baseline or postconcussion neurocognitive test scores, defined operationally as
an ImPACT Impulse Control Composite score of > 30;41
2) self-reported history of special education, speech therapy, repeated year(s) of school, learning disability, attention deficit hyperactivity disorder, dyslexia, or autism; 3)
self-reported history of brain surgery or seizure disorder;
and 4) self-reported history of treatment for drug/alcohol
abuse or psychiatric illness.
Data Collection
All athletes were administered baseline neurocognitive and symptom inventory questionnaires as part of the
ImPACT33 software. ImPACT is a commercially available computerized test for SRC that provides symptom
and neurocognitive test data.33 In addition to neurocognitive scores, ImPACT contains the Total Symptom Score
(TSS), a concussion symptom inventory consisting of 22
items, each rated on a 7-point Likert scale (0–6) for the
presence and severity of postconcussion symptoms.32 The
TSS is an aggregate score of symptom severity (0–132).
Previous studies have established the validity10,42 and reliability32 of the TSS relative to SRC assessment. Raw
scores were recorded for the TSS. All ImPACT baseline
testing was completed prior to each season’s inception in
a controlled, group-setting environment with minimal
distractions.
As pertains to our hypothesis, 2 distinctions were
made when evaluating an athlete’s symptoms:
1) To assess individual symptom severity: This was
a graded phenomenon for each individual symptom. Athletes endorsed the severity of each symptom with 7 possible gradations of that specific symptom, from 0 to 6,
74
with 0 representing symptom absence and 6 reflecting the
most severe.
2) To assess aggregate symptom severity: This was
assessed by summing each individual symptom severity score. For example, to calculate aggregate symptom
severity, if Athlete A rated headache and nausea with a
severity of 5 each, while Athlete B rated headache and
nausea with a severity of 2 each, the aggregate severity
for Athlete A versus B would be 10 versus 4, respectively.
Aggregate symptom severity is equal to the TSS.
Following an SRC, the timing of postconcussion ImPACT testing was dictated by clinical necessity as opposed to a prospective, standardized research protocol.
The primary dependent variable in this study was operationally defined as the number of days until the TSS returned to the athlete’s own baseline TSS index. Using a
reliable change index (RCI) methodology set at the 80%
confidence interval,26 raw change scores equal to or greater than 9.18 points for TSS met criteria for a statistically
significant change. Any difference between postconcussion score and baseline less than these values was defined
as a return to baseline.
Additional data extracted from each de-identified
record included athlete-reported sex, age, years of education, sport, concussion history, and neuropsychiatric
history. Dates of concussion and baseline and postconcussion testing were recorded, which allowed for the calculation of days elapsed between concussion and postinjury testing.
Matching of Sex Cohorts
From the aforementioned clinical database, 740 athletes were identified who had completed valid baseline
ImPACT tests and suffered an SRC. Of these 740 athletes, 112 were excluded from the study based on one of
the following exclusion criteria: special education, speech
therapy, repeated year of school, or learning disability.
Moreover, 96 athletes were not evaluated in the acute period after SRC and did not receive an ImPACT test within
the first 30 days after SRC, leaving 532 eligible athletes.
Exact matching between males and females by number of
prior concussions, age, and days to first postconcussion test
resulted in 244 athletes, with 122 in each group, excluding
288 athletes who were unable to be matched. These results
are summarized in Fig. 1. The male and female cohorts all
met inclusion and exclusion criteria and were successfully
matched based on the number of prior concussions.
The ImPACT scores were analyzed to detect which
athletes returned to symptom baseline within 30 days.
Those athletes who did not return to symptom baseline
within 30 days were excluded from the analysis. In 80%–
90% of SRCs, symptoms last 7–10 days, with recovery
taking slightly longer in children and adolescents.35 We
aimed to confine our study to athletes in the acute, postconcussive period only and exclude those with a protracted recovery, possibly indicative of a minority of patients
experiencing postconcussion syndrome.
Statistical Analysis
Statistical analyses consisted of both descriptive
and inferential procedures for all 22 different symptoms
J Neurosurg: Pediatrics / Volume 13 / January 2014
Sex and sport concussion symptoms
Fig. 1. Flow chart representing participant screening and matching.
used in the ImPACT test. We elected not to use previously described symptom clusters (migraine, cognitive,
neuropsychiatric, and sleep) for fear of missing possible
differences in all 22 symptoms.28,29 Since our project
was devoted specifically to symptoms and did not assess other facets of concussion evaluation (for example,
neurocognitive scores and balance scores), we wanted to
maximize chances of detecting sex-based symptom differences and not risk sacrificing individual symptoms to
symptom clusters. Descriptive statistics were reported as
the mean ± SD for continuous variables, and as frequency
and proportion for categorical variables. The success of
the matching process was evaluated using the t-test of sex
differences on number of prior concussions, age, and days
to postconcussion testing. Means and SD of the ImPACT
symptom scores for both male and female groups were
assessed at baseline and at both postconcussion test dates.
J Neurosurg: Pediatrics / Volume 13 / January 2014
The proportion of participants endorsing symptom
severity was compared between males and females using
Fisher’s exact and chi-square tests. Means and standard deviations of the individual symptom severity and aggregate
symptom severity score (calculated as the sum of severities
of individual symptom scores) for both the male and female groups were assessed at baseline and postconcussion
using the Mann-Whitney U-test. For individual symptom
severity, 22 different symptoms were evaluated; thus statistical significance between groups was evaluated using a
Bonferroni correction at a = 0.05/22 = 0.0023. For aggregate symptom severity, herein known as TSS, one aggregate value was evaluated; thus our alpha value remained at
a = 0.05. For participants returning to baseline, the number
of days to return to baseline TSS using the RCI set at the
80% confidence level was computed. For each TSS, the
mean number of days to return to baseline was compared
75
S. L. Zuckerman et al.
between males and females using the Mann-Whitney Utest. The significance of the difference between the male
and female groups for mean number of days to return to
baseline was evaluated at a = 0.05. None of the participants
included in the final analyses had any missing data. Statistical analyses were performed using IBM SPSS Statistics
(version 20.0.0, IBM Corp.).
in the proportion returning to baseline TSS within 30
days, 119 (97.5%) vs 115 (94.3%), respectively (p = 0.333).
Females took longer to return to symptom baseline
than their male counterparts. The average number of days
to return to baseline TSS was 9.1 ± 7.1 days for females
compared with 7.0 days ± 5.1 days for males (p = 0.013).
These results are presented in Table 4.
Results
Discussion
By design, there were 122 females in the female group
and 122 males in the male group. The groups were matched
on age, and thus the average age in both groups was 16.1
years with similar standard deviations. The female group
had 48 (39.3%) middle school athletes, 67 (54.9%) high
school athletes, and 7 (5.7%) collegiate athletes. The male
group had 42 (34.4%) middle school athletes, 68 (55.7%)
high school athletes, and 12 (9.8%) collegiate athletes. As
might be expected given the sex differences, there were
differences in physical characteristics between males and
females. The mean height, weight, and body mass index
for the female group, respectively, was 65.0 ± 2.7 in, 132.1
± 22.4 lbs, and 22.0 ± 3.2. The same characteristics for the
male group were 69.6 ± 3.8 in, 167.2 ± 43.7 lbs, and 24.0 ±
4.7, respectively. Matching was also completed for concussion history, and both groups had an average of 0.1 ± 0.4
prior concussions. There were differences between males
and females in the sport resulting in concussion. Eightytwo (67.2%) males participated in football compared with
no females. Within the female group, 16 (13.1%) participated in volleyball, 10 (8.2%) participated in softball, and 13
(10.7%) participated in cheerleading, with no participation
by any males in these sports categories. These results are
further summarized in Table 1.
Symptom Severity: Baseline and Postconcussion
At baseline, females reported a greater severity for the
“sleeping less than usual” symptom (0.88 ± 1.49 vs 0.31
± 0.86, p < 0.001) (Table 2). There were no between-sex
differences for all other symptoms, including headache,
nausea, vomiting, balance problems, dizziness, fatigue,
trouble falling asleep, sleeping more than usual, drowsiness, sensitivity to light, sensitivity to noise, irritability,
sadness, nervousness, feeling more emotional, numbness
or tingling, feeling slowed down, feeling mentally foggy,
difficulty concentrating, difficulty remembering, and visual problems.
No differences were found between males and females on postconcussion symptom severity scores. These
results are presented in Table 3.
Sex differences existed in aggregate symptom severity, or TSS. At baseline, females reported greater TSS
(7.24 ± 10.22 vs 4.10 ± 6.52 for males [p = 0.005]). Greater TSS for females was also found postconcussion (21.38
± 19.02 vs 16.80 ± 17.07 for males [p = 0.049]). These
results, which met the a priori alpha of 0.05 level of statistical significance, are presented in Tables 2 and 3.
Return to Baseline Score of Total Symptoms After
Concussion
There was no difference between females and males
76
Sex has emerged as a controversial factor in the assessment and management of athletes after SRC. Empirical studies have yielded conflicting results, with an overall
trend toward increased and longer-lasting symptoms for
females.4,6,12–15,20,38 We endeavored to retrospectively assess acute symptom differences between the sexes before
and after an SRC. First, in our matched cohort, at baseline
females reported higher levels than males of sleeping less
than usual. Postconcussion, there were no sex differences
in any of the 22 individual symptoms. Second, females
experienced an increased aggregate symptom severity, or
TSS, at baseline and postconcussion. Third, concussed female athletes took an average of 2.1 days longer to return
to their preconcussion symptom profile (using reliable
change methodology set at the 80% confidence interval)
compared with concussed male athletes. Overall, our results show little significant variation of individual symptoms between the sexes; however, females endorse higher
symptom severity before and after an SRC. Furthermore,
within the limits of our retrospective design, we noted
that females took longer to return to their symptom baseline than males.
Recent studies on sex differences in the acute postconcussion state have produced mixed results. In agreement with our results, Colvin et al.,12 Broshek et al.,4 and
most recently Covassin et al.13 tested male and female athletes in the acute postconcussive state, and in all cohorts,
females reported a higher number of symptoms than their
male counterparts. Other studies have suggested that
males and females differ in the nature of their symptoms
after concussion.1,18,30,39 Females have been shown to experience more somatic symptoms, such as headache, dizziness, fatigue, and concentration problems than males.
However, our results, using a sample of middle school,
high school, and collegiate athletes, did not confirm these
varying symptom profiles. Except for females sleeping
less than usual, both sex symptom profiles showed no significant differences. This may have been in part due to
our rigorous statistical methods, but may also represent
the benefit of using RCI methodology. Another possibility is that our study included all age ranges, from middle
school to college, and other studies focus primarily on
high school and/or college athletes.
With respect to return to symptom baseline within the
30-day recovery period, we found that female athletes took
an average of 2.1 days longer to return to their baseline
symptom profile compared with concussed male athletes.
Existing data support that male and female athletes may
experience variable recovery trajectories in the postconcussion period. Colvin et al.12 compared 93 male soccer
players with 141 female soccer players ranging in age from
J Neurosurg: Pediatrics / Volume 13 / January 2014
Sex and sport concussion symptoms
TABLE 1: Demographic characteristics of participants (n = 244)
Value*
Characteristic
Female (n = 122)
Male (n = 122)
p Value
mean age in yrs
female sex
school
middle school
high school
college
handedness
right-handedness
ambidexterity
mean height (in inches)
mean weight (in lbs)
mean body mass index
mean no. of yrs of education
mean no. of prior concussions
type of sport
soccer
football
basketball
wrestling
cross-country
tennis
ice hockey
volleyball
baseball
softball
cheerleading
lacrosse
track & field
swimming
mountain biking
rugby
16.1 ± 2.0
122 (100.0)
16.1 ± 2.1
0 (0.0)
0.754
<0.001
48 (39.3)
67 (54.9)
7 (5.7)
42 (34.4)
68 (55.7)
12 (9.8)
0.539
0.841
0.464
110 (90.2)
4 (3.3)
65.0 ± 2.7
132.1 ± 22.4
22.0 ± 3.2
9.7 ± 1.8
0.1 ± 0.4
107 (87.7)
6 (4.9)
69.6 ± 3.8
167.2 ± 43.7
24.0 ± 4.7
9.4 ± 1.9
0.1 ± 0.4
0.779
<0.001
<0.001
<0.001
0.294
>0.999
38 (31.1)
0 (0.0)
20 (16.4)
0 (0.0)
1 (0.8)
1 (0.8)
2 (1.6)
16 (13.1)
0 (0.0)
10 (8.2)
13 (10.7)
7 (5.7)
2 (1.6)
1 (0.8)
1 (0.8)
1 (0.8)
12 (9.8)
82 (67.2)
9 (7.4)
3 (2.5)
0 (0.0)
0 (0.0)
5 (4.1)
0 (0.0)
3 (2.5)
0 (0.0)
0 (0.0)
8 (6.6)
0 (0.0)
0 (0.0)
0 (0.0)
0 (0.0)
8 (6.6)
0 (0.0)
unknown
* Mean values are presented as the mean ± SD. Other values are the number of patients (%).
8 to 24 years and found that females endorsed longer-lasting headaches than their male counterparts. In contrast, a
retrospective, cross-sectional study by Cantu et al.7 demonstrated that the average length of recovery after SRC was
comparable between male and female athletes ranging in
age from 10 to 62 years. Of note, athletes in the study by
Cantu et al. ranged an age span of 52 years, which exceeds
the age range of most studies discussed previously.
Several prior studies have not used RCI methodology. Reliable change index–based scores in SRC research use an athlete as his/her own control, as opposed
to most studies, which focus on mean group sex differences. Symptoms are transient states and vary from day
to day. Reliable change index–based scores take into account normal variability in symptoms from time point to
time point, account for test-retest reliability, and account
J Neurosurg: Pediatrics / Volume 13 / January 2014
for other typical sources of error variance (for example,
practice effects) found in the measurement of human
cognition and behavior. Utilizing RCI-based scores is one
method to account for potentially extraneous sources of
variance in symptom reporting. It may be useful for the
sports medicine researcher to use RCI-based scores in
the assessment of symptoms after an SRC, as reliance on
number and/or ratings of symptom severity alone may not
capture the symptom picture accurately.
Our study has methodological strengths. First, we
addressed many demographic variables (age, concussion
history, education, and time of postconcussion testing)
previously not controlled systematically in prior studies.
Several studies have failed to control for prior number of
concussions, which has been shown to affect symptoms
and scores.11,13 Second, we addressed the symptom vari77
S. L. Zuckerman et al.
TABLE 2: Severity of symptoms at baseline testing
Mean (SD)
Symptom
Female
Male
p Value*
headache
nausea
vomiting
balance problems
dizziness
fatigue
trouble falling asleep
sleeping more than usual
sleeping less than usual
drowsiness
sensitivity to light
sensitivity to noise
irritability
sadness
nervousness
feeling more emotional
numbness or tingling
feeling slowed down
feeling mentally foggy
difficulty concentrating
difficulty remembering
visual problems
TSS†
0.52 (1.07)
0.08 (0.46)
0.01 (0.09)
0.12 (0.42)
0.22 (0.74)
0.47 (1.12)
0.72 (1.36)
0.23 (0.96)
0.88 (1.49)
0.52 (1.17)
0.25 (0.91)
0.16 (0.63)
0.44 (0.91)
0.25 (0.75)
0.50 (1.10)
0.47 (1.08)
0.11 (0.54)
0.18 (0.67)
0.20 (0.59)
0.57 (1.20)
0.18 (0.64)
0.16 (0.55)
7.24 (10.22)
0.33 (0.79)
0.11 (0.48)
0.05 (0.28)
0.09 (0.39)
0.09 (0.39)
0.48 (1.01)
0.50 (1.01)
0.17 (0.65)
0.31 (0.86)
0.32 (0.87)
0.10 (0.47)
0.04 (0.33)
0.25 (0.71)
0.13 (0.56)
0.31 (0.74)
0.20 (0.66)
0.07 (0.28)
0.09 (0.34)
0.05 (0.25)
0.22 (0.69)
0.09 (0.39)
0.11 (0.55)
4.10 (6.52)
0.103
0.681
0.130
0.525
0.086
0.952
0.149
0.586
<0.001
0.123
0.096
0.076
0.061
0.178
0.118
0.019
0.459
0.186
0.008
0.006
0.186
0.559
0.005
* A family-wise p value of 0.05 was obtained by Bonferroni corrected significance level of α = 0.05/22 = 0.0023. A p value of 0.05
was used to assess TSS.
† Mean score per patient.
able more precisely and in several variants, including individual symptom severity and aggregate symptom severity. We found that when these variables were controlled
adequately, the previously noted symptom differences
between males and females disappeared, but the aggregate symptom score differences remained. This study
also used strict tests of statistical significance, which decreased the probability of a false-positive finding due to
multiple comparisons. Finally, we used RCI-based scores,
as opposed to group mean score differences.
Conversely, our study has limitations that bear mentioning. First, this was not a prospective study, but a retrospective cohort study. Variables such as whether the
athlete is in season, school is in session, level of competition, medication status, treatment from a health care professional, and compliance with recommended treatments,
are all potential confounders that could not be controlled
in a retrospective study design. Second, this was a realworld study with no standardized protocol for a post-SRC
testing timeline. Participants completed two post-SRC
ImPACT/TSS tests based on schedule, patient need, and
clinic feasibility, reflecting the variable practices of sports
medicine clinicians. Moreover, differences exist in trainer
and clinician availability between college, high school,
and middle school athletics, which further modify post78
concussion evaluation. Thus, we matched all athletes on
days to postconcussion testing to minimize these inherent
differences. Third, it is possible that our statistical criteria may have been too stringent, potentially obfuscating
trends noted in Results. A larger sample would allow for
this statistical determination, but our rigorous matching
criteria precluded the use of a larger sample. Fourth, we
were unable to control specifically for the sport variable
among our participants. Fifth, all study participants were
from one region of the country. Our study may not be
generalizable to collegiate athletes since such a small
proportion of our subjects (approximately 7%) were collegiate. Similarly, our results may not apply to professional
athletes and may not represent practice in other regions
of the US. Finally, we caution sports medicine clinicians
in concluding that the results of this study suggest that
an additional 2 days of rest for concussed females, as opposed to males, is indicated routinely. It is important to
keep in mind the recommendation of CISG that each concussion is treated individually.
In closing, when assessing the effects of sex after an
SRC, it is incumbent for the health care professional to
appreciate a broader number of variables. Neurocognitive scores were not addressed in our study, as we aimed
to focus solely on symptom reporting, yet are a mainstay
J Neurosurg: Pediatrics / Volume 13 / January 2014
Sex and sport concussion symptoms
TABLE 3: Severity of symptoms at postconcussion testing
Mean (SD)
Symptom
Female
Male
p Value*
headache
nausea
vomiting
balance problems
dizziness
fatigue
trouble falling asleep
sleeping more than usual
sleeping less than usual
drowsiness
sensitivity to light
sensitivity to noise
irritability
sadness
nervousness
feeling more emotional
numbness or tingling
feeling slowed down
feeling mentally foggy
difficulty concentrating
difficulty remembering
visual problems
TSS†
2.58 (1.63)
0.73 (1.30)
0.05 (0.28)
0.98 (1.32)
1.36 (1.53)
1.65 (1.75)
1.13 (1.57)
0.73 (1.39)
0.70 (1.37)
1.67 (1.72)
1.33 (1.51)
1.19 (1.53)
0.90 (1.40)
0.47 (1.03)
0.52 (1.19)
0.72 (1.40)
0.17 (0.66)
0.81 (1.22)
1.06 (1.30)
1.63 (1.68)
0.51 (0.94)
0.49 (0.96)
21.38 (19.02)
2.16 (1.74)
0.63 (1.21)
0.02 (0.20)
0.74 (1.21)
0.97 (1.35)
1.34 (1.61)
0.88 (1.44)
0.37 (0.96)
0.63 (1.26)
1.08 (1.40)
0.98 (1.41)
0.75 (1.21)
0.61 (1.29)
0.24 (0.80)
0.38 (1.06)
0.35 (0.91)
0.15 (0.60)
0.84 (1.33)
0.94 (1.40)
1.52 (1.57)
0.76 (1.24)
0.48 (1.07)
16.80 (17.07)
0.049
0.542
0.436
0.129
0.035
0.160
0.190
0.019
0.698
0.004
0.061
0.008
0.088
0.054
0.335
0.015
0.762
0.881
0.508
0.582
0.072
0.900
0.049
* A family-wise p value of 0.05 was obtained by Bonferroni corrected significance level of α = 0.05/22 = 0.0023. A p value of 0.05
was used to assess TSS.
† Mean score per patient.
of concussion evaluation and management. Although authors have found disparities in male and female neurocognitive scores at baseline3,6,15,43 and postconcussion,4,12,14
a recent study evaluated a homogeneous group of male
versus female soccer players and found no differences
in neurocognitive deficits after SRC.44 With respect to
symptoms, prior studies have shown different symptom
profiles for females and an increased number of symptoms at baseline and postconcussion. Although our study
failed to replicate major symptom differences, we did
TABLE 4: Return to baseline TSS score using RCI scores set at
the 80% confidence interval
Value*
Return to Baseline
Female
Male
p Value†
no. to baseline ≤30 days (%)
mean no. of days
to 1st test
to 2nd test
to baseline
119 (97.5)
115 (94.3)
0.333
4.1 ± 3.1
12.0 ± 6.6
9.08 ± 7.11
4.1 ± 3.1
10.7 ± 5.6
7.04 ± 5.10
>0.999
0.112
0.013
* Mean values are ± SD. Other values are number of patients (%).
† A family-wise p value of 0.05 was used.
J Neurosurg: Pediatrics / Volume 13 / January 2014
confirm a higher level of symptom endorsement and longer return to baseline in females than in males. The results of several recent studies of sex effects on cognition
and symptoms in SRC lead to the preliminary conclusion
that symptoms rather than neurocognitive scores appear
to be the main driver of sex disparities in the sequelae of
SRCs.4,7,12,13,44
The etiology of this disparity is outside the scope
of our study; however, male athletes have been shown
to minimize or deny symptoms to avoid removal from
a game or practice, whereas female athletes show more
concern for their future health.13–15,17,24 Embedded social
biases may be at the heart of symptom variation. If females do in fact more readily report symptoms than
males, it is tantamount to having a more sensitive test for
females than males. In this light, it is no surprise that females have a higher rate and severity of disease. Until we
have an objective measure of symptom recording, rather
than self-report, symptom subjectivity is a potential bias
all future concussion researchers will have to navigate.
Conclusions
Our results demonstrated minor sex differences in
individual symptoms before and after SRC. Females re79
S. L. Zuckerman et al.
ported more symptoms and greater symptom severity at
baseline and post-SRC and, on average, took 2 days longer to return to symptom baseline. Although aspects of
these sex differences in symptoms are statistically significant, the retrospective nature of our study and inherent sex reporting biases must be taken in context when
interpreting our results. Further prospective research is
needed to elucidate the clinical significance of these sex
differences to provide the highest level of medical care to
athletes in the postconcussive period.
Disclosure
Dr. Solomon reports being a consultant for ImPACT. He also
states that he is a member of the ImPACT professional advisory
board and is reimbursed for expenses related to board meetings but
that he did not receive any funding from ImPACT for this study.
Author contributions to the study and manuscript preparation
include the following. Conception and design: Zuckerman, Solomon, Sills. Acquisition of data: Solomon, Sills. Analysis and interpretation of data: Zuckerman, Apple, Odom, Lee, Solomon. Drafting
the article: Zuckerman, Apple, Odom, Lee. Critically revising the
article: all authors. Reviewed submitted version of manuscript: all
authors. Approved the final version of the manuscript on behalf of
all authors: Zuckerman. Statistical analysis: Zuckerman, Odom, Lee,
Solomon. Administrative/technical/material support: Solomon, Sills.
Study supervision: Solomon, Sills.
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Manuscript submitted May 22, 2013.
Accepted September 30, 2013.
Please include this information when citing this paper: published
online November 8, 2013; DOI: 10.3171/2013.9.PEDS13257.
Address correspondence to: Scott L. Zuckerman, M.D., Vanderbilt University Medical Center, Department of Neurological Surgery, T-4224 Medical Center N., Nashville, TN 37232. email: scott.
[email protected].
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