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Sex differences in outcome following sports-related concussion


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Females comprise an increasing percentage of the athlete population across all age groups, and analysis of recent literature reveals that they sustain more concussions in collegiate sports. Results of human and animal studies indicate that females may have poorer outcomes after traumatic brain injury; however, no return-to-play guideline takes sex or other individual differences into account. In the present study the authors evaluated the influence of patient sex on objective neurocognitive performance and subjective reporting of symptoms following sports-related concussion. According to preseason baseline neurocognitive computerized testing in 2340 male and female high school and collegiate athletes, individuals who sustained sports-related concussions (155 persons) were reevaluated using an alternate form of the cognitive test. Sex differences in the magnitude of cognitive change from baseline levels and the subjective experience of symptoms were analyzed. To account for the possible protective effects of helmets, comparisons were performed among females, males with helmets, and males without helmets; none of the female athletes wore helmets. Female athletes had significantly greater declines in simple and complex reaction times relative to preseason baseline levels, and they reported more postconcussion symptoms compared with males. As a group, females were cognitively impaired approximately 1.7 times more frequently than males following concussions. Furthermore, females experienced more objective and subjective adverse effects from concussion even after adjusting for the use of helmets by some groups of male athletes (for example, in football). Return-to-play decisions and concussion management must be objective and made on an individual basis, including consideration of factors such as patient sex rather than relying on a one-size-fits-all guideline.
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S females increasingly participate in sports and other
high-risk activities, a greater understanding of the
role of patient sex in TBI outcome is needed.
1996, 2.4 million high school girls participated in school
sports, representing 39% of the high school athlete popula-
tion. This percentage represents an eightfold increase since
1971 when only 300,000 girls participated in high school
More recent data indicate that females now com
prise 42% of the athlete population at both the high school
and college levels.
Started in 1945, the annual survey of catastrophic foot-
ball injuries was expanded in 1982 through the establish
ment of the National Center for Catastrophic Sports Injury
The expansion was partially motivated by the
increasing participation of female athletes following Title
IX and by the lack of data on catastrophic injuries in female
athletes. Analysis of data collected between 1982 and 1999
revealed that female athletes suffered fatalities or sustained
permanent disabilities while participating in cheerleading,
volleyball, softball, gymnastics, and field hockey and that
more than 50% of these catastrophic injuries occurred due
to cheerleading. In addition, these studies demonstrated that
female athletes are at significant risk of sustaining sports
concussions or more serious brain injuries. Data gathered
by the National Collegiate Athletic Association Injury Sur
veillance System between 1997 and 2000 indicated that
female college athletes experience a greater number of con-
cussions during games than male college athletes, based on
both raw numbers and per game exposure.
These research-
ers found that female collegiate athletes in soccer and bas
ketball sustained significantly more concussions than their
male counterparts. Although several studies have been fo
cused on concussion following sports-related injury, none
has been undertaken to analyze possible sex-based dif
ences in symptom severity
, constellation, or duration.
In the literature on mild head injury in which most trau-
ma is typically due to motor vehicle accidents, there are few
studies that do indicate a greater risk of poor outcome in fe
J Neurosurg 102:856–863, 2005
Sex differences in outcome following
sports-related concussion
Department of Psychiatric Medicine, University of Virginia Health System, Charlottesville, Virginia;
HeadMinder, Inc., New York; Department of Psychiatry, Albert Einstein College of Medicine, New York,
New York; and Department of Psychology, Florida Institute of Technology, Melbourne, Florida
Object. Females comprise an increasing percentage of the athlete population across all age groups, and analysis of recent
literature reveals that they sustain more concussions in collegiate sports. Results of human and animal studies indicate that
females may have poorer outcomes after traumatic brain injury; however, no return-to-play guideline takes sex or other in-
dividual differences into account. In the present study the authors evaluated the influence of patient sex on objective neuro-
cognitive performance and subjective reporting of symptoms following sports-related concussion.
Methods. According to preseason baseline neurocognitive computerized testing in 2340 male and female high school
and collegiate athletes, individuals who sustained sports-related concussions (155 persons) were reevaluated using an alter-
nate form of the cognitive test. Sex differences in the magnitude of cognitive change from baseline levels and the subjec-
tive experience of symptoms were analyzed. To account for the possible protective effects of helmets, comparisons were
performed among females, males with helmets, and males without helmets; none of the female athletes wore helmets.
Female athletes had significantly greater declines in simple and complex reaction times relative to preseason baseline
levels, and they reported more postconcussion symptoms compared with males. As a group, females were cognitively
impaired approximately 1.7 times more frequently than males following concussions. Furthermore, females experienced
more objective and subjective adverse effects from concussion even after adjusting for the use of helmets by some groups
of male athletes (for example, in football).
Conclusions. Return-to-play decisions and concussion management must be objective and made on an individual basis,
including consideration of factors such as patient sex rather than relying on a one-size-fits-all guideline.
KEY WORDS sports-related concussion mild head injury sex-based difference
traumatic brain injury
J. Neurosurg. / Volume 102 / May, 2005
Abbreviations used in this paper: AAN = American Academy
of Neurology; ADHD = attention deficit hyperactivity disorder;
ANOVA = analysis of variance; CI = confidence interval; CRI =
Concussion Resolution Index; CRT = complex reaction time;
LOC = loss of consciousness; MANCOVA = multivariate analysis
of covariance; PS = processing speed; RCI = reliable change in-
dex; SE
= standard error of difference; SRT = simple reaction time;
TBI = traumatic brain injury.
05_05_JNS.1.gls 4/21/05 1:06 PM Page 856
males. Females appear to have a greater likelihood of post-
concussion syndrome at the 1-month follow up,
a greater
incidence of depression following mild TBI,
and a greater
number of persisting symptoms 1 year after mild brain inju-
Although most individuals typically make a full recov-
ery from mild head injury, data from an epidemiological
study at the University of Virginia in the early 1980s re-
vealed that one third of the patients had persisting symp-
toms for at least 3 months.
This result underscored the
importance of studying the phenomenon of mild head in-
jury and identifying characteristics that might relate to de-
layed recovery. Patient sex may be one of the variables that
differentially affects recovery following mild head injury.
Among the literature on TBI are some notable studies
during which investigators examined the role of patient sex
on outcome. It is not surprising that these findings are in
consistent given that the demographic groups and the injury
severity level differ across, and even within, studies.
spite the fact that males have approximately twice the risk
of females for sustaining a TBI,
data from a recent study in
patients with moderate and severe TBI demonstrated that
females had a mortality rate 1.28 times higher than that in
Additionally, the likelihood of a poor outcome in
survivors was 1.57 times higher in females. A metaanal-
ysis on sex-based differences in outcome following TBI
revealed only nine studies in which the authors reported da-
ta according to sex.
Females demonstrated a poorer out-
come in 17 of 20 variables (85%) with a mean effect size
of !0.15. Other researchers, however, have reported that
females are more likely than males to return to school or
work after moderate to severe brain injury.
The as yet limited research on the association between
TBI and sex has yielded contrasting results. In the pediatric
literature, authors of two studies found that girls outper-
formed boys on measures of learning and memory within 1
year after TBI.
In contrast, authors of another study (data
unpublished) found that girls experienced greater dif
ties with executive function following significant brain in
Girls have also been reported to be more vulnerable
to the long-term effects of cranial irradiation and chemo-
Based on a review of the literature and their own
prospective research, Kraus and colleagues
have asserted
that future research in TBI should focus on the effects of sex
as well as the pathophysiological basis of differential out-
comes a
cross the sexes.
Research in animals to investigate sex as a factor in TBI
outcome has also yielded inconsistent results. Authors of
one study found that estrogen treatment in rats before inflic
ting an experimental fluid-percussion brain injury provid-
ed protective ef
fects in males and exacerbated the injury in
Female rats have also been noted to have high-
er mortality rates following fluid-percussion injury
. In hy
ponatremic conditions, depressed oxygen use and cerebral
blood flow were observed in female rodents.
Data from
these animal studies indicated a pathophysiological basis
for the poorer outcome in the female sex following TBI.
More recent research, however, has revealed that estrogen
provided a neuroprotective effect, resulting in a better out-
come in female mice compared with that in the male ones
following experimental TBI inflicted using the murine im-
pact–acceleration head injury method.
In addition, male
mice had a 20% mortality rate, whereas no death occurred
in the female mice.
A principal limitation of the human studies on concus-
sion and TBI is the lack of preinjury data on patients, which
especially limits the scope of research on sex-based dif-
ferences in cognitive functions. For example, results of one
recent study revealed significant sex differences between
male and female college athletes, with females demonstrat-
ing faster and more accurate perceptual motor performance
and better verbal fluency.
Sex differences in neuropsy-
chological test performance in healthy athletes may in turn
obscure sex differences in postconcussion cognitive func-
tioning and recovery. Barth and colleagues
pioneered the
principle of obtaining baseline preseason data on athletes
prior to injury to increase the scope of scientific inquiry into
mild head injury. This methodology, termed the Sports-as-
a-Laboratory model,is widely accepted as the gold stan
dard for identifying and managing sports-related concus
sions and is now common in professional sports and college
In previous studies
we have demonstrated
that the use of RCI scores, a means of appraising injured
athletes individually posttrauma compared with their own
unique baseline scores, is a superior method of determining
and quantifying the severity of postconcussion cognitive
symptoms. W
e therefore hypothesized that a greater under-
standing of potential sex dif
ferences in sports-related con-
cussion would be possible by using a baseline model and
RCI scores.
Clinical Material and Methods
Cognitive Performance Measures
The CRI, a web-based, brief computerized neurocogni-
tive assessment tool, consists of six cognitive subtests that
resolve to three summary speed factors: SRT, CRT, and PS.
The CRI is sensitive to decreases in memory, reaction time,
and speed of information processing immediately following
concussion and until resolution of such typically transient
neurocognitive dysfunction.
All subtests were adminis-
tered before trauma and again at each posttrauma evalua-
tion. Statistical analyses of injured athletes’ test performan-
ces are adjusted for test–retest reliability and for practice
fects. Alternate forms are automatically provided.
When obtaining baseline measures, the subtests were
preceded by a short questionnaire designed to gather demo-
graphic information, concussion history, and other perti-
nent medical information that might be useful in return-to-
play decision making. Following head trauma, the cognitive
subtests were preceded by questions about the athletes
symptom presentation immediately following injury (LOC,
retrograde amnesia, dizziness, headache, and confusion/dis-
orientation), which were answered by the athletic trainer or
team physician who witnessed the injury, and the presence
and intensity of postconcussion symptoms at testing time
(headache, fatigue, memory problems, concentration dif
, nausea, and so forth), which were rated by the athlete.
All symptoms were surveyed at each postconcussion as
sessment. Although many symptoms are often recorded as
absent, mild, moderate, or severe, for our purposes these
symptom scales were truncated to the dichotomy of present
or absent.
Participants and Procedures
Baseline CRI assessments were group administered in
J. Neurosurg. / Volume 102 / May, 2005
Sex differences in outcome from sports-related concussion
05_05_JNS.1.gls 4/21/05 1:06 PM Page 857
computer labs via web-enabled desktop computers to ath-
letes in contact sports at several US high schools and col-
leges as part of an ongoing research project. Institutional re-
view board approval was obtained, as was informed consent
from all adult athletes and from parents of athletes youn-
ger than 18 years of age. Following a concussion, athletes
underwent follow-up tests according to the clinical judg-
ment of the athletic trainer, team physician, or psychologist
in charge of care, typically at 1- to 2-day intervals, until all
symptoms resolved. For the current analysis, only data col-
lected during the first follow up were used for comparisons
with baseline performance levels. No other performances
were included in the analyses.
One hundred fifty-five athletes sustained concussions as
determined at the time of the injury by an athletic trainer or
physician using the Standardized Assessment of Concus
and/or a symptom inventory. Of these athletes, 117
(75.5%) were male and 38 (24.5%) were female. Baseline
cognitive performances on the CRI did not differ according
to patient sex, ethnicity, age (high school compared with
college), or history of learning disability or ADHD. Be-
cause analysis of postconcussion performances on the CRI
according to patient sex was our interest, possible con-
founds were examined. Ethnic representation (Caucasian
compared with non-Caucasian) differed significantly ac-
cording to sex ("
= 8.4, p = 0.004), with Caucasians being
overrepresented in the female group (86.8 compared with
61.5%). Note, however, that results of ANOVA revealed no
difference between ethnic groups on the CRIs at the initial
postconcussion assessment, indicating that potential differ-
ences based on sex would not be confounded by differences
in the ethnic make-up of the two groups. A self-reported
history of a learning disability or ADHD also differed sig-
nificantly according to sex (
= 6.35, p = 0.012), with such
diagnoses being overrepresented in the male group (19.7
compared with 2.6%). Results of ANOVA revealed signifi-
cant differences in postconcussion performances according
to learning disability or ADHD, with those affected by such
disabilities performing significantly slower on two of the
three CRI speed indices (CRT: F = 6.52; df = 1, 153 [sam-
ple size minus two conditions in ANOVA]; p = 0.012
and PS: F = 8.82; df = 1, 153; p = 0.003). Because persons
with a learning disability or ADHD were disproportionate-
ly male, this group of 24 athletes was excluded from further
analyses to avoid confounding findings on sex and con-
Thus, of the 131 athletes studied further, 94 (71.8%) were
males and 37 (28.2%) were females. There was an approx-
imately equal number of high school and college athletes
(47.3 compared with 52.7%, respectively), although women
were overrepresented in the high school group (64.9 com-
pared with 35.1%). Similarly
, although the mean age for the
entire group was 18.72 # 2.1 years (standard deviation,
range 14.3–23.8 years), males were significantly older than
females (19.2 compared with 17.5 years; F = 17.9; df = 1,
129; p
$ 0.001). Because of the age discrepancy, analyses
of age and age-based sex differences were performed for
self-reported symptoms and CRI baseline, follow up, and
baseline follow-up dif
ference scores, with no significant
age or age/sex interactions identified. Sixty-nine percent of
the athletes identified themselves as Caucasian, 23% as Af-
rican-American, and 8% as other. (Note that results of an
ANOVA indicated that in the group excluded for learning
disability and ADHD, there was no difference in baseline
CRI scores based on sex, ethnicity
, or age, thus revealing
that the index is not ethnicity biased.)
In 54% of the athletes,
the incurred injury represented the first ever concussion, in
26% the second, in 11% the third, and in 9% the fourth or
more; these frequencies did not differ significantly accord-
ing to sex. Approximately 75% of the males sustained con-
D. K. Broshek, et al.
J. Neurosurg. / Volume 102 / May, 2005
Summary of sports activities in 131 concussed
athletes grouped according to sex
Group No. of Patients (%)
soccer 13 (35.1)
field hockey 7 (18.9)
lacrosse 5 (13.5)
basketball 4 (10.8)
cheerleading 3 (8.1)
other 5 (13.5)
football 68 (72.3)
lacrosse 6 (6.4)
wrestling 6 (6.4)
other 14 (14.9)
Two indices of concussion severity
grouped according to sex
No. of Patients (%)
Grading Criteria Males Females
Cantu grade
I 45 (47.9) 15 (40.5)
II 22 (23.4) 10 (27.0)
III 27 (28.7) 12 (32.5)
AAN grade
I 10 (10.6) 3 (8.1)
II 67 (71.3) 32 (81.9)
III 17 (18.1) 4 (10.8)
FIG. 1.
Bar graph demonstrating mean RCI scores on CRIs to
gether with 95% CIs on follow up.
Shaded bars represent men;
white bars represent women. * p $ 0.05.
05_05_JNS.1.gls 4/21/05 1:06 PM Page 858
cussions while playing football and 33% of the females did
so while playing soccer. Table 1 details the sports activities
by sex. Males underwent their first postinjury assessment
sooner than did females (mean 2.8 compared with 3.8 days,
respectively; Mann–Whitney
= !2.3, p = 0.021).
Severity of concussion was determined using two meth-
ods, the AAN
and Cantu grading criteria,
which were ap-
plied to each case based on contemporaneous reports by the
athletic trainer or team physician who had witnessed the in-
jury and was involved in the athletes follow-up care. Ta-
ble 2 depicts concussion severity graded according to both
AAN and Cantu criteria stratified by sex. There was no dif-
ference between males and females in injury severity based
on either of these criteria, although males did experience
LOC approximately twice as frequently as females (18
compared with 11%, respectively). In keeping with our pre-
vious research, LOC did not correlate significantly with any
outcome variable.
To assess differences in postconcussion CRI performance
relative to baseline levels, RCI scores were calculated for
the three speed factors in each athlete according to the
following formula: [(x
! x
] (!1).
By multiply-
ing the RCI z score by !1, slower speeds following inju-
ry appeared as negative z scores, and faster postinjury per-
formances as positive ones. T
o test whether there were
differences in postconcussion objective and self-reported
sequelae according to sex, a MANCOVA was performed
using sex as the independent variable, RCI scores for each
of the three CRI speed factors and total number of symp-
toms as dependent variables, and time to follow up as a co-
variate. The time to follow up correlated significantly with
the extent of the cognitive performance decrease compared
with baseline levels regardless of sex; in fact, longer time
periods were associated with more minor decreases. Patient
age, another variable that dif
ferentiated the two groups, did
not correlate with the extent of the performance decrease
compared with baseline, and so was not included as a co-
The overall model was significant for sex (Hotelling T =
0.076, F = 2.36, p = 0.05). Group comparisons were signif-
icant for CRT (F = 5.13, p = 0.025), SRT (F = 6.20, p =
0.014), and number of symptoms (F = 5.41, p = 0.022), but
not for PS (F = 1.41, p = 0.238). Females consistently expe-
rienced greater declines in cognitive function and dem-
onstrated more symptoms. Figure 1 depicts the mean RCI
z scores and 95% CIs for the two sex groups, adjusted
for time to follow up, illustrating the greater performance
declines on the CRI factors in females. In addition to the
three CRI RCI scores, the number of symptoms reported by
athletes at the time of the initial postconcussion evaluation
was treated as a dependent variable reflective of the se-
verity of postconcussion sequelae. The frequency of cogni-
tive impairment based on sex is presented in Fig. 2. Al-
though women reported concentration problems, fatigue,
lightheadedness, and seeing flyspecks significantly more
often than did men, the constellation of symptoms were re-
markably similar between the sexes. Figure 3 depicts the
mean number of symptoms together with 95% CIs reported
by males compared with those reported by females.
To determine the clinical significance of these differen-
ces, athletes were classified as “cognitively impairedif any
one of their RCI scores indicated a decrease of more than
1.645 SE
(p % 0.05) from baseline levels at the postcon-
cussion assessment. A z score of !1.645 was chosen as the
threshold for determining a significant decline from base-
line levels because a decrease of this size is associated with
a probability value of 0.05. Approximately 57% of the fe
males were cognitively impaired compared with 33% of the
males, which represented a significantly greater frequency
= 6.27, p = 0.012).
e hypothesized that females might experience more
J. Neurosurg. / Volume 102 / May, 2005
Sex differences in outcome from sports-related concussion
2. Bar graph depicting self-reported symptoms on follow up according to patient sex.
haded bars
, females. * p $ 0.05.
FIG. 3. Bar graph exhibiting the mean number of symptoms re-
ported on follow up according to patient sex together with 95% CIs.
Shaded bars, males; white bars, females; p $ 0.05.
05_05_JNS.1.gls 4/21/05 1:06 PM Page 859
symptoms and demonstrate significant declines in cognitive
function more frequently than males because few females
wore headgear of any type, whereas most male athletes
were football players, who were equipped with helmets.
Therefore, we divided the male athlete group into those
with and those without helmets and performed a MANCO-
VA using females (all of whom were unhelmeted), unhel
meted males, and helmeted males as the independent vari-
able, the RCIs of the three CRI factors and the number of
symptoms as dependent variables, and the time to follow
up as a covariate. The overall model was significant for the
patient sex helmet variable (Hotelling T = 0.146, F = 2.25,
p = 0.03). Group comparisons were significant for CR
(F = 4.00, p = 0.02), SRT (F = 3.11, p = 0.05), and num-
ber of symptoms (F = 3.74, p = 0.03). Results of pairwise
comparisons indicated that females demonstrated signifi
cantly slower response speed on the CRT and PS, a mar-
ginally slower SRT, and more symptoms compared with
those in unhelmeted males.
Females also had significantly
slower response speed on the SRT and significantly more
symptoms than those in helmeted males, whose perfor-
mance generally occupied a middle ground between the two
groups of unhelmeted athletes. Figure 4 depicts the mean
RCI z scores and 95% CIs for the three groups, adjusted for
time to follow up, illustrating the more severe declines ex
perienced by females on the CRI factors. Figure 5 depicts
the mean number of symptoms with 95% CIs reported by
females, males without helmets, and males with helmets.
To determine the clinical significance of these differen-
ces, athletes were classified as cognitively impaired if any
one of the RCI scores indicated a decrease of more than
1.645 SE
(p % 0.05) from baseline levels at the post-
concussion assessment. Table 3 shows that more than twice
as many unhelmeted females (57%) were cognitively im
paired compared with unhelmeted males (28%), and that
helmeted males experienced impairment in 34% of the
cases. The distribution of these frequencies was significant
= 6.52, p = 0.038). Of additional interest, the Mantel
Haenszel linear-by-linear association value of 5.68 (p =
0.017) indicated that, clinically, the same linear relationship
as that observed in the ANOV
As was present.
Since Title IX was passed in 1972, females have been
participating in sports in increasing numbers. Surprisingly,
the present study appears to be the first effort objectively to
compare neurocognitive sequelae in male and female ath-
letes following sports-related concussion. In this prospec-
tive study in high school and college athletes, we examined
the relationship of patient sex to the severity of cognitive
decline and the number of self-reported symptoms. First,
we identified a significantly more severe decline in females
on measures of SRTs and CRTs, relative to preseason base-
line levels. Second, females self-reported significantly more
symptoms following concussion compared with males.
These sex dif
ferences were evident when comparing males
and females in terms of both the degree of cognitive change
from baseline levels and the frequencies of impaired cog-
nitive performance. In the former case, the decreases in
female cognitive performance levels were approximately
1 SE
greater than those in males. In the latter case, fe-
males were cognitively impaired approximately 1.5 times
more often than males following concussion (57 compared
with 37%, respectively).
These findings did not appear to be
due to dif
ferences in injury severity
, patient age or eth-
nicity, baseline performance levels, or time to follow up. In
fact, females demonstrated significantly greater changes
from baseline cognitive performance and significantly more
symptoms following concussion despite being evaluated a
mean of 24 hours later than males.
Patient age, which did differ between men and women in
our sample, was not significantly correlated with CRI base-
line, follow-up, or baseline follow-up difference scores or
with the number of self-reported symptoms. Furthermore,
D. K. Broshek, et al.
J. Neurosurg. / Volume 102 / May, 2005
. 5. Bar graph demonstrating the mean number of symptoms
as well as CIs reported on follow up by males with helmets
gray bars)
, males without helmets (light gray bars), and females
(white bars). Females had more symptoms than males without hel-
mets, p = 0.01; females had more symptoms than males with hel-
mets, p = 0.05.
IG. 4. Bar graph exhibiting mean RCI scores on CRIs together
with 95% CIs on follow up. *Scores in females (white bars) were
lower than those in males without helmets (light gray bars), p $
0.01; scores in females were lower than those in males with helmets
(dark gray bars), p $ 0.15. **Scores in females were lower than
those in males without helmets, p $ 0.15; scores in females were
lower than those in males with helmets, p
$ 0.05. ***Speeds in fe-
males were lower than those in males without helmets, p $ 0.05.
05_05_JNS.1.gls 4/21/05 1:06 PM Page 860
there was no significant interaction between patient age and
sex for these same scores and symptoms.
An additional hypothesis and a possible explanation for
our findings was that helmets might provide protection for
male athletes, the majority of whom were football players;
however, women experienced more significant sequelae
than helmeted males and suffered more serious symptoms
than males without helmets. Among all unhelmeted ath-
letes, females were more than twice as likely as males to
experience cognitive impairment following concussion (57
compared with 28%, respectively). Based on these data, it
seems clear that females experience more objective and
subjective adverse effects of concussion even after adjusting
for the wearing of protective head gear.
Another possible explanation for the sex-based differ-
ences in our study may be related to the style of play or lev-
el of aggressiveness inherent in different sports. Sports
played by males are typically assumed to be more aggres-
sive, which is part of the reason helmets are often required
even though the same sport played by females does not (for
example, lacrosse), although this theory may not be ac-
curate. Future investigators must examine the sex differen-
ces in the on-field behavior as well as the mechanisms of
sports-related concussion.
From a physiological perspective, sex differences in hor-
monal systems, cerebral organization, and musculature may
partially explain our findings. The literature provides con-
trary findings regarding the potential neural protection af-
forded by female gonadal hormones in animals. Estrogen
may be either a protective or a detrimental factor depending
on the study reviewed, whereas progesterone seems to func-
tion broadly to reduce post-TBI neural impairment.
varying results may be a reflection of study design, includ-
ing whether animals were exposed to a fluid-percussion in-
jury, a focal-impact injury, or an impact-acceleration injury.
In addition, authors of a recent study, which demonstrated
that estrogen provided a neuroprotective effect in female
mice, did not manipulate levels of estrogen but simply ex-
amined differences in recovery based on sex.
In contrast,
other researchers who found that estrogen exacerbated brain
injuries in female rats and provided protective effects in
male rats actually treated the rats with supplemental estro
gen 4 hours prior to inducing head injury.
These discrepant
findings may be partially due to the differential impact of
exogenous compared with endogenous estrogen in TBI. Fu-
ture research in humans should be aimed at examining fluc
tuations in hormonal levels to determine whether there are
cyclical periods of greater vulnerability or greater neuropro
tection in concussed female athletes that might affect neu-
rocognitive outcome, the recovery curve, and the duration
of follow up.
The fact that sex may differentially determine TBI in-
cidence, severity, and symptom resolution should not be
surprising. There are considerable sex-based differences in
neural anatomy and physiology, cerebrovascular organiza-
tion, and cellular response to concussive stimuli. For exam-
ple, cortical neuronal densities are greater in males, where-
as neuropil numbers are greater in females.
Blood flow
rates are greater in females than in males,
and females
exhibit a greater basal rate of glucose metabolism.
The lat-
ter two functional differences may well exist in support
of the increased ionic flux across the greater membrane ar-
ea suggested by the higher neuropil count. To the extent
that brains in females may have greater metabolic demands,
a more intense and prolonged symptom response to mild
TBI may reflect an exacerbated, or at least a more broad-
ly distributed, metabolic cascade as described by Giza and
Specifically, the typical decrease in cerebral blood
flow along with the increased glycemic demands caused by
TBI may interact with the already increased demands and
lead to greater impairment in females than in males.
Although there was no significant sex-based difference in
performance on baseline neurocognitive testing, one of the
limitations of this study is that no inference can be made
about baseline sex differences in intellectual ability or cog-
nitive reserve based on the test administered. It is possible
that any differences might have affected the observed sex
effect in concussion outcome. Furthermore, we only ex-
amined postconcussive sex differences among athletes for
whom we had baseline neurocognitive data, perhaps result-
ing in selection bias. Our study design of obtaining baseline
data in large numbers of athletes in high-risk sports, howev-
er, limits the impact of this confound. In addition, the length
of time between concussion and follow-up neurocognitive
evaluation was not standardized among all the data collec-
tion sites. Interestingly, although female athletes tended not
to be followed up as quickly—thus allowing additional time
for recoverythey still demonstrated poorer outcomes.
Data in this study provide important information for the
clinical management of concussion. Note that although fe
males experienced more severe postconcussion symptoms,
males were followed up significantly sooner (by approxi-
mately 24 hours), perhaps indicating that injuries in females
may not be taken as seriously. Alternatively, this finding
may reflect less aggressive follow-up testing based on the
perceived severity of initial symptoms and conservative
management of the recovery process (that is, not perform
ing cognitive challenges while the patient remains symp
tomatic). Results of previous studies have revealed a ten
dency for females to report more symptoms following head
Those in the medical profession often interpret
such reports as an indication that women complain more de-
spite having fewer objective symptoms. Based on objective
test findings, we assert that females do in fact experience
more severe postconcussion symptoms than males and that
poorer outcomes are not simply due to culturally based sex
ferences in reporting symptoms. Such findings may be
critical in countering the documented reduced levels of
post-TBI services provided to women.
Because more severe objective declines in reaction time
and processing speed mirrored more severe subjective
symptoms, data in this study serve to caution against dis-
missing symptom reports following TBI. Although post-
J. Neurosurg. / Volume 102 / May, 2005
Sex differences in outcome from sports-related concussion
Frequency of cognitive impairment on
postconcussion follow up in 131 athletes*
No. of Patients (%)
Group w/o Cognitive Impairment w/ Cognitive Impairment
unhelmeted males 13 (72.2) 5 (27.8)
helmeted males 50 (65.8) 26 (34.2)
unhelmeted females 16 (43.2) 21 (56.8)
* "
= 6.52, p = 0.038.
05_05_JNS.1.gls 4/21/05 1:06 PM Page 861
concussion syndrome symptoms may represent nonneu-
rological factors,
clearly such is not universally true.
Although male athletes were more likely to experience
LOC at the time of concussion, which may have been inter-
preted as reflecting a more severe injury, women demon-
strated worse cognitive dysfunction on follow up. This find-
ing provides additional evidence for the growing literature
indicating that LOC is not a good predictor of outcome.
Again, our results call into question the return-to-play crite-
ria (such as those of the AAN) that rely heavily on LOC in
grading concussion. Although current investigators still use
LOC as the only measure of severity,
many authors have
pointed out the shortcomings in this approach.
though, intuitively, the approach of using baseline neuro-
cognitive testing to detect changes following concussion ap
pears more sensitive than traditional grading scales, we did
not perform a direct comparison of these two approaches in
the present study
. It remains a critical area for future re-
Female athletes had significantly more severe declines
on SRTs and CRTs relative to preseason baseline levels
and they reported more postconcussion symptoms com-
pared with males. Furthermore, females were cognitively
impaired approximately 1.7 times more often than males
following concussion. Females experienced more objec-
tive and subjective adverse effects of concussion even af-
ter adjusting for the use of helmets by some groups of male
athletes (for example, those playing football). Given the
potential for sex differences and other as yet unidentified
variables that affect concussion severity and recovery
, the
importance of individualized concussion management can-
not be overstated. Data collected on the preseason baseline
administration of computerized or paper-and-pencil neuro-
psychological measures that are validated for detecting con-
cussion for comparison with individual postconcussion da-
ta represent the gold standards for identifying the degree of
cognitive decline and recovery. Medical care and return-to-
play decisions should be based on a comparison between
pre- and postinjury neurocognitive data and the recovery
curve of each individual athlete rather than relying on one-
size-fits-all return-to-play criteria.
Drs. David Erlanger and Tanya Kaushik are employed by Head-
Minder, Inc., which is the publisher of the CRI. Dr. Erlanger also
holds a significant number of shares in the company.
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J. Neurosurg. / Volume 102 / May, 2005
Sex differences in outcome from sports-related concussion
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... There are a variety of factors that influence different outcomes from a concussion for females. Research suggests there is a greater vulnerability for females to have a concussion than males due to neck strength [9,[25][26][27], the neuroanatomy of the brain [9,25,28,29], and the role of the estrogen hormone [9,25,27,29]. Wallace and colleagues studied sex differences in knowledge of concussion symptoms and reporting behavior [22]. ...
... There are a variety of factors that influence different outcomes from a concussion for females. Research suggests there is a greater vulnerability for females to have a concussion than males due to neck strength [9,[25][26][27], the neuroanatomy of the brain [9,25,28,29], and the role of the estrogen hormone [9,25,27,29]. Wallace and colleagues studied sex differences in knowledge of concussion symptoms and reporting behavior [22]. They found that females had higher knowledge of SRC and that males were 4 to 11 times more likely not to report a concussion. ...
Aim: To understand sex differences and sources of concussion education for college students. The literature for college students primarily focuses on sports concussions and general knowledge. Understanding how non-students-athletes learn is critical to developing interventions to improve concussion knowledge. Participants: A random sample of 208 students from four-year institutions. Methods: A 22-question online survey explored postsecondary students' current knowledge and education regarding concussions. Results: Findings indicated that sex differences emerged with concussion knowledge and sources of concussion knowledge (e.g., leaflets, pamphlets, parents, and television). The top choices for where they wanted to learn about concussions were health educators, health centers, and campus peer educators. Conclusion: This study provides an initial evaluation and implications for future research on providing concussion education.
... Once dismissed as a minor, nuisance-type injury (14), a concussion is now regarded as a serious neurological event, the management of which is increasingly prescriptive (15) and, in many states and provinces, legislated (16). More recently, SRC research has begun to focus on gender-related and cultural differences (6,(17)(18)(19)(20). ...
Full-text available
PurposeThere is limited research regarding the characteristics of those from the general population who seek care following acute concussion.Methods To address this gap, a large cohort of 473 adults diagnosed with an acute concussion (female participants = 287; male participants = 186) was followed using objective measures prospectively over 16 weeks beginning at a mean of 5.1 days post-injury.ResultsFalls were the most common mechanism of injury (MOI) (n = 137, 29.0%), followed by sports-related recreation (n = 119, 25.2%). Male participants were more likely to be injured playing recreational sports or in a violence-related incident; female participants were more likely to be injured by falling. Post-traumatic amnesia (PTA) was reported by 80 participants (16.9 %), and loss of consciousness (LOC) was reported by 110 (23.3%). In total, 54 participants (11.4%) reported both PTA and LOC. Male participants had significantly higher rates of PTA and LOC after their injury compared to their female counterparts. Higher initial symptom burden was associated with a longer duration of recovery for both male and female participants. Female participants had more symptoms and higher severity of symptoms at presentation compared to male participants. Female participants were identified to have a longer recovery duration, with a mean survival time of 6.50 weeks compared to 5.45 weeks in male participants (p < 0.0001). A relatively high proportion of female and male participants in this study reported premorbid diagnoses of depression and anxiety compared to general population characteristics.Conclusion Although premorbid diagnoses of depression and/or anxiety were associated with higher symptom burden at the initial visit, the duration of symptoms was not directly associated with a pre-injury history of psychological/psychiatric disturbance. This cohort of adults, from the general population, seeking care for their acute concussion attained clinical and functional recovery over a period of 4–12 weeks.
... Studies on sex differences in TBI have mostly reported that females sustain concussions more often than males, 11,12 have worse outcomes, 68,69 a different symptom constellation and a delayed resolution of symptoms. [69][70][71] These sex-related differences cannot be solely explained by psychiatric history, sociodemographic variables or care pathways, alone. 72 Findings from this study may provide some fresh insight into the biomechanical basis of TBI sex differences. ...
Existing axonal finite element models do not consider sex morphological differences or the fidelity in dynamic input. To facilitate a systematic investigation into the micromechanics of diffuse axonal injury, we develop a parameterized modeling approach for automatic and efficient generation of sex-specific axonal models according to specified geometrical parameters. Baseline female and male axonal models in the corpus callosum with random microtubule (MT) gap configurations are generated for model calibration and evaluation. They are then used to simulate a realistic tensile loading consisting of both a loading and a recovery phase (to return to an initial undeformed state) generated from dynamic corpus callosum fiber strain in a real-world head impact simulation. We find that MT gaps and the dynamic recovery phase both critical to successfully reproduce MT undulation as observed experimentally, which has not been reported before. This strengthens confidence in model dynamic responses. A statistical approach is further employed to aggregate axonal responses from a large sample of random MT gap configurations for both female and male axonal models (N=10,000 each). We find that peak strains in MTs and the Ranvier node and associated neurofilament failures in female axons are substantially higher than those in male axons due to fewer MTs in the former and the random nature of MT gap locations. Despite limitations in various model assumptions due to limited experimental data currently available, these findings highlight the need to systematically characterize MT gap configurations and to ensure a realistic model input for axonal dynamic simulations. Finally, this study may offer fresh and improved insight into the biomechanical basis of sex differences in brain injury and sets the stage for more systematic investigations at the microscale in the future, both numerically and experimentally.
... Despite these limitations, these results contribute to the increasing literature surrounding differing outcomes between sexes following concussion, which include symptom presentation and recovery time. [25][26][27][28][29] Future research could evaluate if clinicians provide differing recommendations for physical activity to male versus female athletes after concussion, or if there are sex differences in access to exercise equipment or venues, contributing to differing physical activity behaviors and recovery outcomes. ...
Context: Early physical activity (PA) after concussion may promote symptom resolution. Prior studies have investigated exercise frequency/duration, yet precise PA intensity or volume required for optimal recovery requires further investigation. moderate to vigorous physical activity (MVPA) is beneficial for physical health. We investigated whether sedentary time, light activity time, MVPA time, or activity frequency in the weeks following concussion are associated with time to symptom resolution among adolescents. Design: Prospective cohort study. Methods: Adolescents 10-18 years of age were tested ≤14 days of concussion and followed until symptom resolution. At the initial visit, participants rated symptom severity and were provided wrist-worn activity trackers to monitor PA for the following week. PA behavior was categorized each day based on heart rate: sedentary (resting), light PA (50%-69% age-predicted max heart rate), and MVPA (70%-100% age-predicted max heart rate). Symptom resolution was defined as the date when participants reported cessation of concussion-like symptoms. Patients were not given specific PA instructions, though some may have received instructions from their physician. Results: Fifty-four participants were included in the study (54% female; mean age = 15.0 [1.8] y; initially assessed 7.5 [3.2] d after concussion). Female athletes recorded more sedentary time (900 [46] vs 738 [185] min/d; P = .01; Cohen d = 0.72), and less time in light PA (194.7 [64.5] vs 224 [55] min/d; P = .08; Cohen d = 0.48) and MVPA (23 [17] vs 38 [31] min/d; P = .04; Cohen d = 0.58) than male athletes. After adjusting for sedentary time, hours per day with >250 steps, sex, and initial symptom severity, more MVPA time was associated with faster symptom resolution time (hazard ratio = 1.016; 95% confidence interval, 1.001-1.032; P = .04). Conclusion: Our findings offer preliminary insight into how varying PA intensities affect concussion recovery, as MVPA may be a higher intensity than what is typically prescribed in concussion care.
Objectives: To examine level of play (LOP) as a risk factor for concussion severity and recovery-related outcomes among high school athletes, stratified by sex, and among boys, by sport (football, non-football male sports). Design/setting: Secondary analysis of data collected through the High School Reporting Information Online surveillance system for academic years 2007-2008 through 2018-2019. Participants: A total of 9916 concussions were reported between the academic years 2007-2008 and 2018-2019 from 9 sports (5189 from football; 2096 from non-football male sports; 2631 from female sports). Main outcome measure: Examined the association between LOP (Freshman, Junior Varsity [JV], and Varsity teams) and concussion outcomes (number of concussion symptoms, symptom resolution time [SRT], and time to return to play [RTP]). Results: Compared with Varsity football athletes, concussed JV football athletes had on average 0.19 fewer concussion symptoms, longer SRT (>1 week vs <1 week: odds ratio [OR] = 1.3; 95% confidence interval [CI], 1.1-1.5), and longer RTP (1-3 weeks vs <1 week: OR = 1.5; 95% CI, 1.2-1.9; >3 weeks vs <1 week: OR = 1.6; 95% CI, 1.1-2.3). Compared with Varsity football athletes, Freshman football athletes had on average 0.48 fewer concussion symptoms, longer SRT (OR = 1.3; 95% CI, 1.1-1.5), and longer RTP (1-3 weeks vs <1 week: OR = 1.5; 95% CI, 1.1-2.0; >3 weeks vs <1 week: OR = 2.0; 95% CI, 1.3-3.0). Similarly, compared with female athletes on Varsity teams, concussed JV female athletes had longer RTP (1-3 weeks vs <1 week: OR = 1.8; 95% CI, 1.2-2.7). Trend analyses revealed an increase in the number of concussion symptoms between 2015-2016 and 2018-2019, a decrease between 2009-2010 and 2018-2019 for SRT of less than 1 week, and an increase between 2014-2015 and 2018-2019 for RTP of less than 1 week among Varsity football athletes. Among Varsity female athletes, there was a linear decrease during the study period for RTP of less than 1 week. Conclusions: Despite a higher number of symptoms overall and in recent years, Varsity football players had shorter RTP than Freshman and JV athletes.
College students' beliefs and attitudes concerning concussion, and masculinity norms, were examined in relation to stigma and willingness to seek treatment for possible concussion. Beliefs were measured using a revised Illness Perception Questionnaire (IPQ). Participants: Participants were 631 undergraduates at a Northeastern university, most of whom were nonathletes with no concussion. Methods: Data were collected online. Regression analysis were performed to identify predictors of stigma and treatment willingness. Results: Beliefs that concussion symptoms reflect malingering, are controllable, and have psychological causes were related to more stigmatizing attitudes, as was endorsement of masculinity norms regarding winning and risk-taking. Believing that concussion symptoms are long-lasting and endorsing competitiveness, pain discounting, and self-reliance predicted willingness to seek treatment. Preliminary structural models showed adequate fit. Conclusions: In addition to beliefs assessed by the IPQ, traditional conceptions of masculinity warrant greater attention in the study of concussion-related stigma and willingness to seek treatment.
Objectives: The purpose of this study is to evaluate the utilityof the Patient-Reported Outcomes Measurement Information System (PROMIS)anxiety and depressive symptom domains [1] in conjunction with the Post-Concussion SymptomScale (PCSS) [2] for identifying pediatric patients withemotional symptoms following a concussion, and to identify predictors of higheremotional symptom loads. Methods: We recruited English-speaking patients aged 8-17 years presenting to a tertiary-care concussion clinic from 2014 to 2018 (n = 458). Demographics and clinical data including PCSS, injury date, previous history of anxiety/depression, and Vestibular/Ocular-Motor Screen (VOMS) were collected from patients' electronic medical records. Participants completed surveys in the PROMISTM Pediatric Item Bank v1.1-Anxiety and Depressive Symptoms domains at their initial clinic visit. Multivariable linear regression identified predictors of higher emotional symptom loads. Results: Overall, 425 (92.8%) reported ≥ 1 emotional symptom on either PROMIS or PCSS. Predictors of higher emotional symptom loads were abnormal VOMS, female sex, history of anxiety or depression, and longer time since injury. Conclusion: Our results suggest that adding PROMIS anxiety and depressive symptom surveys to pediatric concussion evaluations may identify more children with emotional symptoms, allowing clinicians to better direct post-concussion treatment and incorporate psychological support for patients if necessary. Future studies should examine whether earlier identification of emotional symptoms with these tools facilitates recovery and improves short- and/or long-term psychological outcomes in pediatric concussions.
Introduction/Purpose We tested the hypothesis that an objective measure of auditory processing reveals a history of head trauma that does not meet the clinical definition of concussion. Methods Division I collegiate student-athletes ( n = 709) across 19 sports were divided into groups, based on their sport, using prevailing classifications of “contact” (317 males, 212 females) and “noncontact” (58 males, 122 females). Participants were evaluated using the frequency-following response (FFR) to speech. The amplitude of FFR activity in a frequency band corresponding to the fundamental frequency (F0)—the voice pitch—of the speech stimulus, an outcome reduced in individuals with concussions, was critically examined. Results We found main effects of contact level and sex. The FFR-F0 was smaller in contact athletes than noncontact athletes and larger in females than males. There was a contact by sex interaction, with the FFR-F0 of males in the contact group being smaller than the three other groups. Secondary analyses found a correlation between FFR-F0 and length of participation in contact sports in male athletes. Conclusion These findings suggest that the disruption of sensory processing in the brain can be observed in individuals without a concussion but whose sport features regular physical contact. This evidence identifies sound processing in the brain as an objective marker of subconcussion in athletes.
Objective: The purpose of this study was to investigate the clinical presentation (using PCSS), mechanism of injury, and recovery time of concussions sustained by gymnasts. Methods: A retrospective chart review was performed at Boston Children's Hospital: Sports Medicine Clinic. Patients were identified with the words 'gymnastics' and 'concussion.' Male and female gymnasts were included if they sustained a concussion during gymnastics training or competition and were between the ages of 6-22 years old. Sex, age, injury site, diagnosis, mechanism of injury, and time to presentation are described. Patients were compared during different types of gymnastics events for overall symptom burden, and individual symptom severities. Results: A total of 201 charts were assessed over a 6-year period and 62 patients met inclusion criteria. Floor exercise was the most common event at the time of injury. Loss of consciousness occurred in 20% of injuries. There was no significant association between the type of event and PCSS upon initial clinical visit (p = 0.82). A total of 13 gymnasts returned to the clinic for a subsequent injury after their concussion (Table 3). Conclusions: Gymnasts are at risk for sport-related concussions. Most gymnasts reporting to a tertiary care center with the diagnosis of concussion sustain their injuries during floor exercise.
Full-text available
The study consisted of a prospective investigation of 45 consecutively admitted patients who had sustained a mild head injury. In all cases the duration of post-traumatic amnesia was less than 24 hours. Head injury patients had an average of three adverse life events in the year preceding injury compared with 1.5 for controls. Using the PSE, 39% of the group were diagnosed psychiatric cases at six weeks after the injury. For cases the mean level of chronic social difficulties (3.3) was four times that for non-cases (0.8). Six months after injury, 28% of the head injury group had three or more symptoms. These chronic cases were on average ten years older than those whose symptoms had remitted. Chronic cases had, on average, three social difficulties, twice as many as found among those whose symptoms had remitted. The emergence and persistence of the postconcussional syndrome are associated with social adversity before the accident. While young men are most at risk of minor head injury, older women are most at risk of chronic sequelae.
In brief: Cerebral concussion occurs frequently in contact sports; more than 250,000 concussions occur annually in football alone. Definitions and classifications of severity of concussion vary, which makes evaluation of data extremely difficult. By combining elements of various definitions, the author has developed a practical, on-the-field grading scheme for identifying concussion in contact sports (grade 1: mild, with no loss of consciousness; grade 2: moderate, with less than five minutes of unconsciousness or more than 30 minutes of posttraumatic amnesia; grade 3: severe, with five or more minutes of unconsciousness or 24 or more hours of posttraumatic amnesia). Also discussed are management of concussion and guidelines for determining when an athlete may safely return to play.
The Concussion Resolution Index (CRI) is an online assessment tool designed to track resolution of symptoms following sports-related concussion. The CRI is composed of six subtests measuring reaction time, visual recognition, and speed of information processing. Three factors are derived from the subtests: Simple Reaction Time (SRT), Complex Reaction Time (CRT), and Processing Speed (PS). Multiple alternate forms within subtests afford simple, reliable, assessment of change, relative to a baseline test completed by an athlete. The test also assesses self-reported neurophysiological symptoms at the time of injury and tracks resolution of these symptoms. The data demonstrate the CRI is a valid and reliable measure of cognitive performance in a relatively heterogeneous group of athletes aged 13–35. Two methods of statistical analysis for assessing change from baseline were compared to establish a psychometric basis for return-to-play decision-making: the Reliable Change Index (RCI) and multiple regression. Multiple regression was more accurate than the RCI in determining a decline in performance relative to the baseline.