Article Text
Abstract
Objectives To examine sex differences in sport-related concussion (SRC) across comparable sports.
Methods Prospective cohort of collegiate athletes enrolled between 2014 and 2017 in the Concussion Assessment, Research and Education Consortium study.
Results Among 1071 concussions (females=615; 57.4%), there was no difference in recovery (median days to full return to play) (females=13.5 (IQR 9.0, 23.1) vs males=11.8 (IQR 8.1, 19.0), p=0.96). In subgroup analyses, female recovery was longer in contact (females=12.7 days (IQR 8.8, 21.4) vs males=11.0 days (IQR 7.9, 16.2), p=0.0021), while male recovery was longer in limited contact sports (males=16.9 days (IQR 9.7, 101.7) vs females=13.8 days (IQR 9.1, 22.0), p<0.0001). There was no overall difference in recovery among Division I schools (females=13.7 (IQR 9.0, 23.1) vs males=12.2 (IQR 8.2 19.7), p=0.5), but females had longer recovery at the Division II/III levels (females=13.0 (IQR 9.2, 22.7) vs males=10.6 (IQR 8.1, 13.9), p=0.0048).
Conclusion Overall, no difference in recovery between sexes across comparable women’s and men’s sports in this collegiate cohort was found. However, females in contact and males in limited contact sports experienced longer recovery times, while females had longer recovery times at the Division II/III level. These disparate outcomes indicate that, while intrinsic biological sex differences in concussion recovery may exist, important, modifiable extrinsic factors may play a role in concussion outcomes.
- concussion
- female
- gender
- male
- sports analysis in different types of sports
Data availability statement
Data are available upon reasonable request.
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Introduction
Differences between women and men in sport-related concussion (SRC) have been described, with some studies indicating that females have longer symptom recovery,1–4 and greater time loss from sports, compared with males.5 6 The data are heterogeneous, however, with other studies reporting similar recovery between sexes.7–9 The relative contributions of intrinsic biological sex versus extrinsic sociocultural or gendered behavioural differences are unclear. Conflicting results likely reflect a complex interaction of factors that are important to disentangle in order to identify modifiable risk factors that could improve disparities in concussion recovery between sexes.
Advances have been made in our understanding of the intrinsic biological differences between females and males that may influence concussion recovery. Female axons in the central nervous system are smaller in diameter and mechanically more prone to stretch injury than male axons.10 Males exhibit greater white matter volume and higher cortical neuronal densities compared with females.11 Intrinsic differences in neck strength may confer a greater risk of concussion for females who have lower neck strength.12 Females are more likely to report symptoms, when healthy or after concussion,11 13–15 although it is unclear whether this is due to intrinsic biological differences, greater injury severity, or sociocultural, gendered-reporting behaviours.11 16 17
Extrinsic factors, including different rules of play, variations in training practices and use of safety equipment, may also play a role in sex differences in SRC. In lacrosse, rule differences prohibit intentional body checking for women, where a greater proportion of females sustain concussions in games compared with males and are more likely sustain a concussion due to contact with an object, such as the stick or ball, rather than another player.7 18 In contrast, in soccer and ice hockey, no sex differences have been found in mechanism of injury, which is player-to-player contact for both sexes.19 20 Similarly, differences in level of athletic trainer or sports medicine support may also play a role in differences in SRC recovery. Delays in care have been shown to influence sex differences in concussion recovery,21 and recovery for athletes in general,22–24 making early access to athletic training and sports medical care another important modifiable extrinsic factor. These extrinsic factors represent opportunities for intervention to narrow gaps in concussion outcomes between sexes.
To this end, the aim of this study was to compare preinjury and injury characteristics, as well as recovery, defined as the time to full return to play (RTP) from SRC, in a large cohort of athletes participating in collegiate sports where both single-sex women’s and men’s teams are fielded, in order to determine what differences may exist. Examining comparable sports may help disentangle intrinsic and extrinsic factors, in particular those that may be modifiable, to help mitigate risk of concussion injury and improve time to recovery.
Methods
Study design and procedures
Data for this investigation were obtained from an ongoing prospective cohort study, the Concussion Assessment, Research and Education (CARE) Consortium, sponsored by the National Collegiate Athletic Association (NCAA) and the Department of Defense. A detailed, in-depth description of the CARE Consortium structure and standard procedures have been previously published.25 26 In brief, after providing written informed consent, varsity-level collegiate athletes at 30 institutions enrolled during the study period between 2014 and 2017 were assessed during the preseason using a standardised battery of symptom-based, clinical and neuropsychological measures. Concussion care across all sites was conducted according to standardised study protocol. Concussions that occurred within games or practices and reported at the time of game or practice to the team athletic trainer were documented as ‘reported immediately’. In addition to daily symptom assessments, injured athletes had standardised study evaluations performed after injury by a trained athletic trainer under the supervision of the team physician according to study protocol at one timepoint within 48 hours, again when initiating the RTP process and on conclusion of the RTP protocol when cleared for full RTP. The primary outcome for this study was recovery as defined as days to full RTP.
Preinjury data for this analysis included standard demographic information for each athlete, including previous concussion(s) and premorbid health conditions, as well as preinjury assessments—the Sport Concussion Assessment Tool-3 (SCAT3) symptom questionnaire and the Brief Symptom Inventory-18 (BSI-18). Postinjury data consisted of standardised details of injury (eg, mechanism and setting), loss of consciousness, post-traumatic amnesia, postinjury SCAT3 and BSI scores. Recovery outcomes included time to return to academics and full RTP.
Study participants
Female and male varsity-level athletes of the CARE Consortium were included in this study if (1) they sustained a concussion while participating in an NCAA sport fielding both single-sex women’s and men’s teams (ie, excluding American football, wrestling and field hockey) and (2) there were sufficient numbers of concussions among both sexes in order to make meaningful comparisons (see figure 1). Participant sex was self-identified. Sport contact level was defined as previously published25 with contact sports including basketball, diving, ice hockey, lacrosse, soccer and water polo; limited contact sports including baseball/softball, cheerleading, gymnastics, volleyball, cross-country/track, and field events; and non-contact sports including swimming and tennis.25 26
Patient and public involvement
Feedback from previous student athletes regarding study procedures was incorporated into the study design to account for participant burden and current student athletes were involved in supporting the recruitment of other student athletes into the current study.
Data analysis
Each characteristic (ie, demographics, preinjury characteristics, injury setting, injury characteristics, recovery outcomes) was compared between sexes using χ2 analyses on the categorical variables of interest and Kruskal-Wallis analysis on the continuous variables. Kaplan-Meier estimates were used to compare time to full RTP for females and males, both overall and by level of contact (contact, limited contact and non-contact), within sex, as well as between division level of play.26
Results
Demographics and preinjury characteristics
During the study period, a total of 3354 concussions occurred. Excluding concussions in non-NCAA sports (mostly service academy cadets participating in club sports), concussions occurring in sports where only a women’s or men’s team is fielded, concussions in sports where too few occurred to make statistically meaningful comparisons, repeat concussions, concussions without baseline testing and non-sports concussions left 1071 athletes (57.4% female) meeting inclusion criteria (see figure 1). A significantly greater proportion of females had a history of migraines compared with males (females=12% vs males=6%, p=0.001). Preseason SCAT3 symptom burden was higher among females (3 (IQR 0, 9)) relative to males (1 (IQR 0, 4), p<0.0001), as was BSI somatisation scores (females=0 (IQR 0, 1) vs males=0 (IQR 0, 0), p<0.0001). Despite the narrow range of symptom scores on both scales, the differences between females and males remained highly significant. No other significant differences in demographic and preinjury characteristics were found between cohorts (see table 1).
Injury characteristics
Injury characteristics are described in table 1. Compared with males, a greater number of injuries in females occurred in practice rather than games (females=68.0% vs males=58.6%, p=0.0019). Almost 75% of injuries sustained by males were in a contact sport, whereas only slightly over 50% of females sustained their injury in a contact sport (females=55.0% vs males=72.0%, p<0.001). The most common mechanism of injury for females was contact with an object, such as a ball, puck or stick (29.3%), whereas the most common mechanism for males was collision with an opponent (35.2%, p<0.001). Slightly over half of all athletes reported their injury immediately (females=51.9% vs males=56.9%, p=0.2). At the first postinjury evaluation, females reported higher SCAT3 symptom severity scores than males (females=13 (IQR 3, 32) vs males=7 (IQR 1, 20), p<0.001), as well as higher BSI scores (females=2 (IQR 0, 4); males=0 (IQR 0, 2), p<0.0001). Presence of post-traumatic amnesia at the time of injury was significantly more common in males compared with females (10.2% vs 5.8%, p<0.05), while there was no difference between sexes in loss of consciousness at injury.
Recovery characteristics
When examining the overall cohort, there was no statistically significant difference between the sexes in recovery (median days to full RTP) (females=13.5 (IQR 9.0, 23.1) and males=11.8 (IQR 8.1, 19.0), p=0.96; figure 2). In contrast, when examining recovery by level of contact, contact sport females had longer recovery (contact females=12.7 (IQR 8.8, 21.4) vs males=11.0 (IQR 7.9, 16.2); p=0.0021), while limited contact males had longer recovery (limited contact females=13.8 (IQR 9.0, 22.0) vs males=16.9 (IQR 9.7, 101.7); p<0.0001) (see figure 3). While most athletes returned directly to full-time academics (74.3%), a greater proportion of females returned to academics gradually, rather than fully all at once (females=22.0% vs males=13.0%, p<0.01).
We examined recovery within sex, comparing levels of contact, as well as between sex, by division level of play (Division I vs Division II/III). We found that, among females, non-contact athletes had longer recovery (non-contact=17.4 (IQR 1.2, 29.7) vs limited contact=13.8 (IQR 9.0, 22.0) vs contact=12.7 (IQR 8.8, 21.4), p=0.017). In contrast, among males, limited contact athletes had longer recovery (limited contact=16.9 (IQR 9.7, 101.7) vs contact=11.0 (IQR 7.9, 16.2) vs non-contact=12.2 (IQR 9.2, 17.7), p<0.0001) (see figure 4). When examining by division level of play, there were no differences in recovery between sexes at the Division I level (females=13.7 (IQR 9.0, 23.1) vs males=12.2 (IQR 8.2, 19.7), p=0.5). However, at the Division II/III level, females had longer recovery than males (females=13.0 (IQR 9.2, 22.7) vs males=10.6 (IQR 8.1, 13.9), p=0.0048) (see figure 5).
Discussion
Differences in SRC recovery between females and males participating in collegiate sports remain incompletely understood, with conflicting reports in the literature, likely due to a combination of intrinsic and extrinsic factors. Further examination of the characteristics of SRC among comparable men’s and women’s sports could improve our understanding of the relative contribution of these intrinsic and extrinsic factors on observed differences. Such an understanding could inform efforts to modify extrinsic factors to narrow any gap in recovery outcomes between the sexes. This study examined a large prospective cohort of collegiate athletes participating in comparable sports fielding both single sex women’s and men’s teams. Our sample size enables the robust characterisation of important demographic preinjury, injury and recovery characteristics that could shed light on differences between sexes.
Similarities between sexes
Importantly, no statistically significant difference was observed between the sexes regarding recovery (time to full RTP) in this investigation. This is notable in light of the greater preinjury and postinjury symptom burden among the females in this cohort, a characteristic which has been previously described in the literature as a risk factor for longer recovery times.1–4 Our findings indicate that, while greater preinjury symptom burden may be related to intrinsic biological differences between the sexes both before and after injury, it may be mitigated by extrinsic factors, resulting in overall similar times to recovery in this cohort. Previous studies have shown that the modifiable extrinsic factor of early access to specialised concussion medical care has an effect on concussion outcomes, with earlier specialised care translating into improved recovery times.21–24 The rate of immediate reporting of concussion between sexes was similar (56.9% of males and 51.9% of females), implying that delayed presentation for concussion care is not likely to be the relevant extrinsic factor at play here, although delayed presentation has been identified as a risk factor for longer recovery times in other studies. The equity in concussion reporting between the sexes in this cohort may, in part, be accounted for by the fact that all of the athletes in this cohort were competing at institutions with robust athletic training and sports medicine programmes, as well as participating in the CARE Consortium, reflecting an environment with an enhanced level of concussion awareness and attention. These factors may partly explain the overall similar recovery observed between the sexes. In light of this, we must consider that Title IX, the historic 1972 Federal civil rights law prohibiting discrimination based on sex in education programmes receiving Federal funding, may be an extrinsic factor that has helped to level the playing field for women in terms of access to collegiate athletics and in access to specialised athletic training support and sports medical care, thereby mitigating risk for longer concussion recovery associated with female sex.
Differences between sexes
Despite comparable times for overall recovery between sexes, our study does identify some differences in recovery between certain subgroups. Across sex, females had longer recovery in contact sports, while males had longer recovery in limited contact sports. Within sex, non-contact females and limited contact males both took longer to recover than their same-sex counterparts. When examining RTP by level of contact, both women and men in contact sports returned to play sooner than their non-contact and limited contact counterparts. This suggests that extrinsic factors (ie, either external pressure to return to contact sport or increased access to athletic training and sports medical care due to contact sport participation) are influencing RTP. Further research is warranted to disentangle these factors. Considering these results, it seems unlikely that intrinsic biological sex differences entirely account for these findings, indicating that any biological sex differences that may exist are interacting with extrinsic factors.
One such extrinsic factor may be disparities in resource allocation among college athletic teams. High-risk collision men’s sports generally use more resources with on-field athletic training coverage for all practices and games, while women’s sports and lower contact men’s sports may have fewer resources allocated and immediately available. Increased immediate access to sports medical care can provide more active acute management, which has been shown to improve time to symptom recovery, especially females, representing an extrinsic factor influencing concussion recovery outcomes.21 23 24 With emerging evidence that immediate recognition and identification of concussion and removal from play,22 and early access to specialised care with active management, such as supervised aerobic exercise, play an important role in shortening recovery time in both youth and collegiate sports,24 26 27 our finding of seemingly paradoxical longer recovery for men in limited contact sports compared with men in contact and non-contact sports may represent a tangible manifestation of disparities due to differential resource allocation affecting outcomes. The additional finding that men and women had similar rates of recovery at the Division I level but that sex differences emerge at the Division II and III levels further raises this issue that perhaps these resource-related extrinsic factors may play a role in these findings. Indeed, recent research indicates that the ratio of athletic training and medical clinicians to athletes systematically differs between division levels of play and may affect injury outcomes in general.28–30 Further investigation is warranted to disentangle the effect that these modifiable extrinsic factors may have on any differences in concussion outcomes within or between the sexes among men and women participating in comparable sports.
Additional sex differences in recovery from concussion were noted. While most athletes usually returned to school full time without a graded progression, a greater proportion of females returned to academics more gradually (22% vs 13%). This may represent a social construct of gendered behaviour,31 with women taking a more careful approach to return to academics, or a biological difference in physiological recovery with females having greater symptom burden precluding immediate full return to academics. This question cannot be answered by our investigation. Since the most recent consensus statement from the Concussion in Sport Group recommends a return to learn protocol for athletes in general,32 our results indicate that this may be particularly helpful when managing female collegiate athletes.
We also confirmed previously described findings that females report greater levels of symptomatology at both the preinjury and postinjury timepoints and found a higher prevalence of self-reported migraines among the concussed women, both of which have been previously reported and appear to be associated with greater risk of concussion and longer recovery.1–6 The reproducibility and robustness of these findings across multiple studies, including our large and diverse cohort, indicate a likely biological basis for these sex differences. This makes our finding of overall similar recovery times between females and males even more notable.
Regarding injury characteristics, as others have described,28 29 33 34 post-traumatic amnesia occurred more commonly among the males in our cohort, while there was no difference in rates of loss of consciousness. It is unclear whether this reflects differences in mechanism of injury (player vs object) resulting in differential magnitude of experienced forces or severity of the injury itself. Compared with males, females more commonly sustained their injuries in practice than in competition, potentially presenting another opportunity for primary prevention, by identifying and altering risky training practices for women’s sports. In football, reducing contact and modifying drills in practice have resulted in fewer practice-related concussions for men.30 35 36 By examining more closely how concussions occur in practice for women’s sports, interventions that result in changes in training could potentially reduce the occurrence of concussions in practice for women.
Limitations of our cohort study are that we cannot determine causation, but can only report on associations and demographic and symptom-based assessments are limited by athlete self-report. The relevance of these results may also be limited to the collegiate setting. The level of attention that athletes in this study received may be greater than what is typical for comparable collegiate athletes, but this only further reinforces our conclusions: that greater levels of attention to concussion may mitigate any biologically based sex differences in concussion outcomes. Future studies should examine more closely the role of various extrinsic factors that might influence sex-based differences in concussion with the goal of developing interventions to reduce those disparities.
Conclusions
In comparable collegiate sports where both single-sex teams are fielded, there were no overall differences between sexes regarding time to full RTP. However, when examining sports by contact level, females in contact sports had longer recovery than men, while men in limited contact sports had longer recovery than women. Female athletes at the Division II/III level of competition had longer recovery than male athletes while their Division I counterparts demonstrated no differences in recovery from males. Within sex, males in limited contact sports had longer recovery compared with full contact or non-contact male athletes, while females in non-contact sports had longer recovery compared with limited and full contact female athletes. Females sustained a higher proportion of concussions in practice compared with men who sustained more concussions in competition. These data indicate that, while intrinsic factors of biological sex may play a role, there are likely multiple modifiable extrinsic factors, such as altering training practices and rules of play, as well as increasing access to athletic training and sports medical staff, that may further close the gap in concussion outcomes between women and men across all sports.
What are the findings?
Overall, there was no difference in recovery between females and males with respect to time to full return to play (RTP) across comparable sports where single-sex teams of both sexes are fielded.
On subgroup analysis, no difference in recovery between females and males was noted at the Division I level, but females had longer recovery times at the Division II/III level.
Females had longer time to RTP in contact sports compared with males in contact sports, and compared with other females in limited and non-contact sports. Males had longer time to RTP in limited contact sports compared with females in limited contact sports and other males in contact and non-contact sports, likely reflecting both extrinsic and intrinsic influences resulting in differences.
These differences in outcomes between the sexes likely reflect a combination of intrinsic factors related to both biological sexes, as well as modifiable extrinsic factors such as training procedures, rules of play and availability of medical resources, such as athletic training and sports medical coverage.
How might it impact on clinical practice in the future?
Identifying training procedures and rules of play that can be changed may represent modifiable extrinsic factors that can improve concussion outcomes for all athletes by reducing the incidence of concussion.
Re-examination of institutional policies to more equitably reallocate resources (athletic training and sports medical staff availability) between women’s and men’s sports teams at the collegiate level to improve early concussion identification, diagnosis and active management may modify an important extrinsic factor to close any gap in concussion outcomes due to biological sex.
Data availability statement
Data are available upon reasonable request.
Ethics statements
Patient consent for publication
Ethics approval
This study was approved by the Human Research Protection Office and the Institutional Review Boards at each participating institution.
Acknowledgments
Contributing CARE Consortium investigators include: Scott Anderson, ATC (University of Oklahoma); Holly J Benjamin, MD (University of Chicago); Alison Brooks, MD, MPH (University of Wisconsin-Madison); Thomas Buckley, PhD and Thomas Kaminski, PhD (University of Delaware); Kenneth Cameron, PhD, MPH, ATC (United States Military Academy); James R Clugston, MD, MS (University of Florida); Michael Collins, PhD and Anthony P Kontos, PhD (University of Pittsburgh Medical Center); Stefan Duma, PhD and Steve Rowson, PhD (Virginia Tech); James T Eckner, MD, MS (University of Michigan); Carlos Estevez, DPT and Christopher Gardner, MS PA-c (United States Coast Guard Academy); Luis A Feigenbaum, DPT, ATC (University of Miami); Joshua T Goldman, MD (UCLA); Megan Houston, PhD, ATC and Steven Svoboda, MD (West Point); April Hoy, MS, ATC (Azusa Pacific University); Jonathan Jackson, MD and Gerald McGinty, DPT (United States Air Force Academy); Louise A Kelly, PhD (California Lutheran University); Laura Lintner, DO (Winston-Salem University); Jason P Mihalik, PhD, CAT(C), ATC (University of North Carolina at Chapel Hill); Jessica Miles, PhD, ATC (University of North Georgia); Christopher M Miles, MD (Wake Forest University); Justus D Ortega, PhD (Humboldt State University); Nicholas Port, PhD (Indiana University); Margot Putukian, MD (Princeton University); Julianne D Schmidt, PhD, ATC (University of Georgia); Adam Susmarski, MD (United States Naval Academy). The authors would also like to thank the athletes, research and medical staff at each of the participating sites as well as the staff of the CARE Consortium.
References
Footnotes
Twitter @drtinamaster
Contributors CLM made substantial contributions to the conception of the study, the acquisition and interpretation of data, drafting the work, revising it critically for important intellectual content, providing final approval of the version published and is accountable for all aspects of the work. BK, ML and WZ made substantial contributions to the conception of the study, the analysis and interpretation of data, revising it critically for important intellectual content and providing final approval of the version published. KBA, MAMC, TMA, PFP and SB made substantial contributions to the conception of the study, the acquisition and interpretation of data, revising the manuscript critically for important intellectual content, providing final approval of the version published and are accountable for all aspects of the work. CARE Consortium investigators HJB, MAB, TAB, KC, JC, MWC, SD, JTE, CAE, LF, CG, JG, MNH, AH, JCJ, TWK, LAK, AK, LL, GTMG, JPM, JM, CM, JO, NP, MP, SR, JDS, AJS and SJS made substantial contributions to the acquisition of data, revising it critically for important intellectual content and providing final approval of the version published.
Funding This publication was made possible, in part, by support from the Grand Alliance Concussion Assessment, Research and Education (CARE) Consortium, funded by the National Collegiate Athletic Association (NCAA) and the Department of Defense (DoD). The US Army Medical Research Acquisition Activity, Fort Detrick, MD is the awarding and administering acquisition office. This work was supported by the Office of the Assistant Secretary of Defense for Health Affairs through the Psychological Health and Traumatic Brain Injury Program under award number W81XWH-14-2-0151.
Competing interests None declared.
Patient and public involvement Patients and/or the public were involved in the design, or conduct, or reporting, or dissemination plans of this research. Refer to the Methods section for further details.
Provenance and peer review Not commissioned; externally peer reviewed.