Effect of sex on symptoms and return to baseline in sport-related concussion

Clinical article

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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.

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.

Abstract

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.

Every 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 (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 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 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.

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, 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.

Fig. 1.
Fig. 1.

Flow chart representing participant screening and matching.

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 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.

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 α = 0.05/22 = 0.0023. For aggregate symptom severity, herein known as TSS, one aggregate value was evaluated; thus our alpha value remained at α = 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 between males and females using the Mann-Whitney U-test. The significance of the difference between the male and female groups for mean number of days to return to baseline was evaluated at α = 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.).

Results

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. Eighty-two (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.

TABLE 1:

Demographic characteristics of participants (n = 244)

CharacteristicValue*p Value
Female (n = 122)Male (n = 122)
mean age in yrs16.1 ± 2.016.1 ± 2.10.754
female sex122 (100.0)0 (0.0)<0.001
school
 middle school48 (39.3)42 (34.4)0.539
 high school67 (54.9)68 (55.7)0.841
 college7 (5.7)12 (9.8)0.464
handedness
 right-handedness110 (90.2)107 (87.7)
 ambidexterity4 (3.3)6 (4.9)0.779
mean height (in inches)65.0 ± 2.769.6 ± 3.8<0.001
mean weight (in lbs)132.1 ± 22.4167.2 ± 43.7<0.001
mean body mass index22.0 ± 3.224.0 ± 4.7<0.001
mean no. of yrs of education9.7 ± 1.89.4 ± 1.90.294
mean no. of prior concussions0.1 ± 0.40.1 ± 0.4>0.999
type of sport
 soccer38 (31.1)12 (9.8)
 football0 (0.0)82 (67.2)
 basketball20 (16.4)9 (7.4)
 wrestling0 (0.0)3 (2.5)
 cross-country1 (0.8)0 (0.0)
 tennis1 (0.8)0 (0.0)
 ice hockey2 (1.6)5 (4.1)
 volleyball16 (13.1)0 (0.0)
 baseball0 (0.0)3 (2.5)
 softball10 (8.2)0 (0.0)
 cheerleading13 (10.7)0 (0.0)
 lacrosse7 (5.7)8 (6.6)
 track & field2 (1.6)0 (0.0)
 swimming1 (0.8)0 (0.0)
 mountain biking1 (0.8)0 (0.0)
 rugby1 (0.8)0 (0.0)
 unknown8 (6.6)0 (0.0)

Mean values are presented as the mean ± SD. Other values are the number of patients (%).

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.

TABLE 2:

Severity of symptoms at baseline testing

SymptomMean (SD)p Value*
FemaleMale
headache0.52 (1.07)0.33 (0.79)0.103
nausea0.08 (0.46)0.11 (0.48)0.681
vomiting0.01 (0.09)0.05 (0.28)0.130
balance problems0.12 (0.42)0.09 (0.39)0.525
dizziness0.22 (0.74)0.09 (0.39)0.086
fatigue0.47 (1.12)0.48 (1.01)0.952
trouble falling asleep0.72 (1.36)0.50 (1.01)0.149
sleeping more than usual0.23 (0.96)0.17 (0.65)0.586
sleeping less than usual0.88 (1.49)0.31 (0.86)<0.001
drowsiness0.52 (1.17)0.32 (0.87)0.123
sensitivity to light0.25 (0.91)0.10 (0.47)0.096
sensitivity to noise0.16 (0.63)0.04 (0.33)0.076
irritability0.44 (0.91)0.25 (0.71)0.061
sadness0.25 (0.75)0.13 (0.56)0.178
nervousness0.50 (1.10)0.31 (0.74)0.118
feeling more emotional0.47 (1.08)0.20 (0.66)0.019
numbness or tingling0.11 (0.54)0.07 (0.28)0.459
feeling slowed down0.18 (0.67)0.09 (0.34)0.186
feeling mentally foggy0.20 (0.59)0.05 (0.25)0.008
difficulty concentrating0.57 (1.20)0.22 (0.69)0.006
difficulty remembering0.18 (0.64)0.09 (0.39)0.186
visual problems0.16 (0.55)0.11 (0.55)0.559
TSS7.24 (10.22)4.10 (6.52)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.

No differences were found between males and females on postconcussion symptom severity scores. These results are presented in Table 3.

TABLE 3:

Severity of symptoms at postconcussion testing

SymptomMean (SD)p Value*
FemaleMale
headache2.58 (1.63)2.16 (1.74)0.049
nausea0.73 (1.30)0.63 (1.21)0.542
vomiting0.05 (0.28)0.02 (0.20)0.436
balance problems0.98 (1.32)0.74 (1.21)0.129
dizziness1.36 (1.53)0.97 (1.35)0.035
fatigue1.65 (1.75)1.34 (1.61)0.160
trouble falling asleep1.13 (1.57)0.88 (1.44)0.190
sleeping more than usual0.73 (1.39)0.37 (0.96)0.019
sleeping less than usual0.70 (1.37)0.63 (1.26)0.698
drowsiness1.67 (1.72)1.08 (1.40)0.004
sensitivity to light1.33 (1.51)0.98 (1.41)0.061
sensitivity to noise1.19 (1.53)0.75 (1.21)0.008
irritability0.90 (1.40)0.61 (1.29)0.088
sadness0.47 (1.03)0.24 (0.80)0.054
nervousness0.52 (1.19)0.38 (1.06)0.335
feeling more emotional0.72 (1.40)0.35 (0.91)0.015
numbness or tingling0.17 (0.66)0.15 (0.60)0.762
feeling slowed down0.81 (1.22)0.84 (1.33)0.881
feeling mentally foggy1.06 (1.30)0.94 (1.40)0.508
difficulty concentrating1.63 (1.68)1.52 (1.57)0.582
difficulty remembering0.51 (0.94)0.76 (1.24)0.072
visual problems0.49 (0.96)0.48 (1.07)0.900
TSS21.38 (19.02)16.80 (17.07)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.

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 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.

TABLE 4:

Return to baseline TSS score using RCI scores set at the 80% confidence interval

Return to BaselineValue*p Value
FemaleMale
no. to baseline ≤30 days (%)119 (97.5)115 (94.3)0.333
mean no. of days
 to 1st test4.1 ± 3.14.1 ± 3.1>0.999
 to 2nd test12.0 ± 6.610.7 ± 5.60.112
 to baseline9.08 ± 7.117.04 ± 5.100.013

Mean values are ± SD. Other values are number of patients (%).

A family-wise p value of 0.05 was used.

Discussion

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 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 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 variable 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 real-world 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 postconcussion 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 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 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 reported 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.

References

  • 1

    Adler A: Mental symptoms following head injury. Arch Neurol Psychiatry 53:34431945

  • 2

    Alves WMColohan ARO'Leary TJRimel RWJane JA: Understanding posttraumatic symptoms after minor head injury. J Head Trauma Rehabil 1:1121986

  • 3

    Barr WB: Neuropsychological testing of high school athletes. Preliminary norms and test-retest indices. Arch Clin Neuropsychol 18:911012003

  • 4

    Broshek DKKaushik TFreeman JRErlanger DWebbe FBarth JT: Sex differences in outcome following sports-related concussion. J Neurosurg 102:8568632005

  • 5

    Broshek DKSamples HBeard JGoodkin HP: Current practices of the child neurologist in managing sports concussion. J Child Neurol [epub ahead of print]2012

  • 6

    Brown CNGuskiewicz KMBleiberg J: Athlete characteristics and outcome scores for computerized neuropsychological assessment: a preliminary analysis. J Athl Train 42:5155232007

  • 7

    Cantu RCGuskiewicz KRegister-Mihalik JK: A retrospective clinical analysis of moderate to severe athletic concussions. PM R 2:108810932010

  • 8

    Cantu RCRegister-Mihalik JK: Considerations for return-to-play and retirement decisions after concussion. PM R 3:10 Suppl 2S440S4442011

  • 9

    Capruso DXLevin HS: Cognitive impairment following closed head injury. Neurol Clin 10:8798931992

  • 10

    Chen JKJohnston KMCollie AMcCrory PPtito A: A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. J Neurol Neurosurg Psychiatry 78:123112382007

  • 11

    Collins MWGrindel SHLovell MRDede DEMoser DJPhalin BR: Relationship between concussion and neuropsychological performance in college football players. JAMA 282:9649701999

  • 12

    Colvin ACMullen JLovell MRWest RVCollins MWGroh M: The role of concussion history and gender in recovery from soccer-related concussion. Am J Sports Med 37:169917042009

  • 13

    Covassin TElbin RJHarris WParker TKontos A: The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. Am J Sports Med 40:130313122012

  • 14

    Covassin TSchatz PSwanik CB: Sex differences in neuropsychological function and post-concussion symptoms of concussed collegiate athletes. Neurosurgery 61:3453512007

  • 15

    Covassin TSwanik CBSachs MKendrick ZSchatz PZillmer E: Sex differences in baseline neuropsychological function and concussion symptoms of collegiate athletes. Br J Sports Med 40:9239272006

  • 16

    Covassin TSwanik CBSachs ML: Sex differences and the incidence of concussions among collegiate athletes. J Athl Train 38:2382442003

  • 17

    Dick RW: Is there a gender difference in concussion incidence and outcomes?. Br J Sports Med 43:Suppl 1i46i502009

  • 18

    Edna THCappelen J: Late post-concussional symptoms in traumatic head injury. An analysis of frequency and risk factors. Acta Neurochir (Wien) 86:12171987

  • 19

    Englander JHall KStimpson TChaffin S: Mild traumatic brain injury in an insured population: subjective complaints and return to employment. Brain Inj 6:1611661992

  • 20

    Farace EAlves WM: Do women fare worse: a metaanalysis of gender differences in traumatic brain injury outcome. J Neurosurg 93:5395452000

  • 21

    Faul MDXu LWald MMCoronado VG: Traumatic Brain Injury in the United States: Emergency Department Visits Hospitalizations and Deaths 2002–2006 AtlantaCenters for Disease Control and Prevention2010

  • 22

    Frommer LJGurka KKCross KMIngersoll CDComstock RDSaliba SA: Sex differences in concussion symptoms of high school athletes. J Athl Train 46:76842011

  • 23

    Gessel LMFields SKCollins CLDick RWComstock RD: Concussions among United States high school and collegiate athletes. J Athl Train 42:4955032007

  • 24

    Granito VJ Jr: Psychological response to athletic injury: gender differences. J Sport Behav 25:2432592002

  • 25

    Hootman JMDick RAgel J: Epidemiology of collegiate injuries for 15 sports: summary and recommendations for injury prevention initiatives. J Athl Train 42:3113192007

  • 26

    Iverson GLLovell MRCollins MW: Interpreting change on ImPACT following sport concussion. Clin Neuropsychol 17:4604672003

  • 27

    Julie GKELikang XLisa CM: Nonfatal traumatic brain injuries from sports and recreation activities—United States, 2001–2005. MMWR Morb Mortal Wkly Rep 56:7337372007

  • 28

    Lau BCCollins MWLovell MR: Cutoff scores in neurocognitive testing and symptom clusters that predict protracted recovery from concussions in high school athletes. Neurosurgery 70:3713792012

  • 29

    Lau BCCollins MWLovell MR: Sensitivity and specificity of subacute computerized neurocognitive testing and symptom evaluation in predicting outcomes after sports-related concussion. Am J Sports Med 39:120912162011

  • 30

    Lidvall HFLinderoth BNorlin B: Causes of the post-concussional syndrome. Acta Neurol Scand Suppl 56:31441974

  • 31

    Lincoln AECaswell SVAlmquist JLDunn RENorris JBHinton RY: Trends in concussion incidence in high school sports: a prospective 11-year study. Am J Sports Med 39:9589632011

  • 32

    Lovell MRIverson GLCollins MWPodell KJohnston KMPardini D: Measurement of symptoms following sports-related concussion: reliability and normative data for the postconcussion scale. Appl Neuropsychol 13:1661742006

  • 33

    Maroon JCLovell MRNorwig JPodell KPowell JWHartl R: Cerebral concussion in athletes: evaluation and neuropsychological testing. Neurosurgery 47:6596722000

  • 34

    McCrory PMeeuwisse WJohnston KDvorak JAubry MMolloy M: Consensus statement on concussion in sport – The 3rd International Conference on Concussion in Sport held in Zurich, November 2008. PM R 1:4064202009

  • 35

    McCrory PMeeuwisse WHAubry MCantu BDvorák JEchemendia RJ: Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med 47:2502582013

  • 36

    National Collegiate Athletic Association: 1981–82—2008–09 NCAA Sports Sponsorship and Participation Rates Report Indianapolis, INNational Collegiate Athletic Association2010

  • 37

    Powell JWBarber-Foss KD: Traumatic brain injury in high school athletes. JAMA 282:9589631999

  • 38

    Preiss-Farzanegan SJChapman BWong TMWu JBazarian JJ: The relationship between gender and postconcussion symptoms after sport-related mild traumatic brain injury. PM R 1:2452532009

  • 39

    Rutherford WH: Sequelae of concussion caused by minor head injuries. Lancet 1:141977

  • 40

    Ryan LMWarden DL: Post concussion syndrome. Int Rev Psychiatry 15:3103162003

  • 41

    Schatz PMoser RSSolomon GSOtt SDKarpf R: Prevalence of invalid computerized baseline neurocognitive test results in high school and collegiate athletes. J Athl Train 47:2892962012

  • 42

    Schatz PPardini JELovell MRCollins MWPodell K: Sensitivity and specificity of the ImPACT Test Battery for concussion in athletes. Arch Clin Neuropsychol 21:91992006

  • 43

    Weiss ESiedentopf CMHofer ADeisenhammer EAHoptman MJKremser C: Sex differences in brain activation pattern during a visuospatial cognitive task: a functional magnetic resonance imaging study in healthy volunteers. Neurosci Lett 344:1691722003

  • 44

    Zuckerman SLSolomon GSForbes JAHaase RFSills AKLovell MR: Response to acute concussive injury in soccer players: is gender a modifying factor? Clincal article. J Neurosurg Pediatr 10:5045102012

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Article Information

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.zuckerman@vanderbilt.edu.

Please include this information when citing this paper: published online November 8, 2013; DOI: 10.3171/2013.9.PEDS13257.

© AANS, except where prohibited by US copyright law.

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Figures

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    Flow chart representing participant screening and matching.

References

1

Adler A: Mental symptoms following head injury. Arch Neurol Psychiatry 53:34431945

2

Alves WMColohan ARO'Leary TJRimel RWJane JA: Understanding posttraumatic symptoms after minor head injury. J Head Trauma Rehabil 1:1121986

3

Barr WB: Neuropsychological testing of high school athletes. Preliminary norms and test-retest indices. Arch Clin Neuropsychol 18:911012003

4

Broshek DKKaushik TFreeman JRErlanger DWebbe FBarth JT: Sex differences in outcome following sports-related concussion. J Neurosurg 102:8568632005

5

Broshek DKSamples HBeard JGoodkin HP: Current practices of the child neurologist in managing sports concussion. J Child Neurol [epub ahead of print]2012

6

Brown CNGuskiewicz KMBleiberg J: Athlete characteristics and outcome scores for computerized neuropsychological assessment: a preliminary analysis. J Athl Train 42:5155232007

7

Cantu RCGuskiewicz KRegister-Mihalik JK: A retrospective clinical analysis of moderate to severe athletic concussions. PM R 2:108810932010

8

Cantu RCRegister-Mihalik JK: Considerations for return-to-play and retirement decisions after concussion. PM R 3:10 Suppl 2S440S4442011

9

Capruso DXLevin HS: Cognitive impairment following closed head injury. Neurol Clin 10:8798931992

10

Chen JKJohnston KMCollie AMcCrory PPtito A: A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. J Neurol Neurosurg Psychiatry 78:123112382007

11

Collins MWGrindel SHLovell MRDede DEMoser DJPhalin BR: Relationship between concussion and neuropsychological performance in college football players. JAMA 282:9649701999

12

Colvin ACMullen JLovell MRWest RVCollins MWGroh M: The role of concussion history and gender in recovery from soccer-related concussion. Am J Sports Med 37:169917042009

13

Covassin TElbin RJHarris WParker TKontos A: The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. Am J Sports Med 40:130313122012

14

Covassin TSchatz PSwanik CB: Sex differences in neuropsychological function and post-concussion symptoms of concussed collegiate athletes. Neurosurgery 61:3453512007

15

Covassin TSwanik CBSachs MKendrick ZSchatz PZillmer E: Sex differences in baseline neuropsychological function and concussion symptoms of collegiate athletes. Br J Sports Med 40:9239272006

16

Covassin TSwanik CBSachs ML: Sex differences and the incidence of concussions among collegiate athletes. J Athl Train 38:2382442003

17

Dick RW: Is there a gender difference in concussion incidence and outcomes?. Br J Sports Med 43:Suppl 1i46i502009

18

Edna THCappelen J: Late post-concussional symptoms in traumatic head injury. An analysis of frequency and risk factors. Acta Neurochir (Wien) 86:12171987

19

Englander JHall KStimpson TChaffin S: Mild traumatic brain injury in an insured population: subjective complaints and return to employment. Brain Inj 6:1611661992

20

Farace EAlves WM: Do women fare worse: a metaanalysis of gender differences in traumatic brain injury outcome. J Neurosurg 93:5395452000

21

Faul MDXu LWald MMCoronado VG: Traumatic Brain Injury in the United States: Emergency Department Visits Hospitalizations and Deaths 2002–2006 AtlantaCenters for Disease Control and Prevention2010

22

Frommer LJGurka KKCross KMIngersoll CDComstock RDSaliba SA: Sex differences in concussion symptoms of high school athletes. J Athl Train 46:76842011

23

Gessel LMFields SKCollins CLDick RWComstock RD: Concussions among United States high school and collegiate athletes. J Athl Train 42:4955032007

24

Granito VJ Jr: Psychological response to athletic injury: gender differences. J Sport Behav 25:2432592002

25

Hootman JMDick RAgel J: Epidemiology of collegiate injuries for 15 sports: summary and recommendations for injury prevention initiatives. J Athl Train 42:3113192007

26

Iverson GLLovell MRCollins MW: Interpreting change on ImPACT following sport concussion. Clin Neuropsychol 17:4604672003

27

Julie GKELikang XLisa CM: Nonfatal traumatic brain injuries from sports and recreation activities—United States, 2001–2005. MMWR Morb Mortal Wkly Rep 56:7337372007

28

Lau BCCollins MWLovell MR: Cutoff scores in neurocognitive testing and symptom clusters that predict protracted recovery from concussions in high school athletes. Neurosurgery 70:3713792012

29

Lau BCCollins MWLovell MR: Sensitivity and specificity of subacute computerized neurocognitive testing and symptom evaluation in predicting outcomes after sports-related concussion. Am J Sports Med 39:120912162011

30

Lidvall HFLinderoth BNorlin B: Causes of the post-concussional syndrome. Acta Neurol Scand Suppl 56:31441974

31

Lincoln AECaswell SVAlmquist JLDunn RENorris JBHinton RY: Trends in concussion incidence in high school sports: a prospective 11-year study. Am J Sports Med 39:9589632011

32

Lovell MRIverson GLCollins MWPodell KJohnston KMPardini D: Measurement of symptoms following sports-related concussion: reliability and normative data for the postconcussion scale. Appl Neuropsychol 13:1661742006

33

Maroon JCLovell MRNorwig JPodell KPowell JWHartl R: Cerebral concussion in athletes: evaluation and neuropsychological testing. Neurosurgery 47:6596722000

34

McCrory PMeeuwisse WJohnston KDvorak JAubry MMolloy M: Consensus statement on concussion in sport – The 3rd International Conference on Concussion in Sport held in Zurich, November 2008. PM R 1:4064202009

35

McCrory PMeeuwisse WHAubry MCantu BDvorák JEchemendia RJ: Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med 47:2502582013

36

National Collegiate Athletic Association: 1981–82—2008–09 NCAA Sports Sponsorship and Participation Rates Report Indianapolis, INNational Collegiate Athletic Association2010

37

Powell JWBarber-Foss KD: Traumatic brain injury in high school athletes. JAMA 282:9589631999

38

Preiss-Farzanegan SJChapman BWong TMWu JBazarian JJ: The relationship between gender and postconcussion symptoms after sport-related mild traumatic brain injury. PM R 1:2452532009

39

Rutherford WH: Sequelae of concussion caused by minor head injuries. Lancet 1:141977

40

Ryan LMWarden DL: Post concussion syndrome. Int Rev Psychiatry 15:3103162003

41

Schatz PMoser RSSolomon GSOtt SDKarpf R: Prevalence of invalid computerized baseline neurocognitive test results in high school and collegiate athletes. J Athl Train 47:2892962012

42

Schatz PPardini JELovell MRCollins MWPodell K: Sensitivity and specificity of the ImPACT Test Battery for concussion in athletes. Arch Clin Neuropsychol 21:91992006

43

Weiss ESiedentopf CMHofer ADeisenhammer EAHoptman MJKremser C: Sex differences in brain activation pattern during a visuospatial cognitive task: a functional magnetic resonance imaging study in healthy volunteers. Neurosci Lett 344:1691722003

44

Zuckerman SLSolomon GSForbes JAHaase RFSills AKLovell MR: Response to acute concussive injury in soccer players: is gender a modifying factor? Clincal article. J Neurosurg Pediatr 10:5045102012

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