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. Author manuscript; available in PMC: 2023 Nov 1.
Published in final edited form as: Sports Med. 2022 Jul 6;52(11):2759–2773. doi: 10.1007/s40279-022-01719-7

Age of First Concussion and Cognitive, Psychological, and Physical Outcomes in NCAA Collegiate Student Athletes

Jena N Moody 1, Jasmeet P Hayes 1,2, Thomas A Buckley 3, Julianne D Schmidt 4, Steven P Broglio 5, Thomas W McAllister 6, Michael McCrea 7, Paul F Pasquina 8, Jaclyn B Caccese 2,9; CARE Consortium Investigators
PMCID: PMC9833421  NIHMSID: NIHMS1860035  PMID: 35794432

Abstract

Objective

Concussions are common among youth athletes and could disrupt critical neurodevelopment. This study examined the association between age of first concussion (AFC) and neurocognitive performance, psychological distress, postural stability, and symptoms commonly associated with concussion in healthy collegiate men and women student athletes.

Methods

Participants included 4267 collegiate athletes from various contact, limited-contact, and non-contact sports (1818 women and 2449 men) who completed baseline assessments as part of the Concussion Assessment, Research and Education (CARE) Consortium. Psychological distress was assessed with the Brief Symptom Inventory 18; neurocognitive performance was assessed with the Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT); symptoms commonly associated with concussion were assessed with the ImPACT Post-Concussion Symptom Scale; postural stability was assessed with the Balance Error Scoring System. Generalized linear models were used to examine the effects of AFC on clinical outcomes separately in men and women.

Results

Later AFC was associated with lower global (Exp(B) = 0.96, P = 0.001) and somatic (Exp(B) = 0.96, P = 0.002) psychological distress on the Brief Symptom Inventory 18 and faster ImPACT reaction time (B = − 0.003, P = 0.001) in women. AFC was not associated with any clinical outcomes in men.

Conclusion

Younger AFC was associated with some differences in psychological distress and reaction time among women but not men; however, these results are likely not clinically meaningful. Sociodemographic disparities, pre-existing conditions, and sport type may impact clinical and cognitive outcomes in collegiate athletes more than concussion history. Future work should examine the relationship between AFC and lifespan-related outcomes.

1. Introduction

Concussions result from a force transmitted to the head or body and are often accompanied by clinical symptoms including headache, dizziness, and confusion [1]. Concussions are a prominent health concern in the USA, specifically among youth athletes. The Centers for Disease Control and Prevention estimate that there are 1.6–3.8 million sport- and recreation-related concussions in the USA each year [2], with 65% of all sports-related concussions occurring in youth ages 5–18 years [3]. Understanding the future cognitive, psychological, and physical consequences of concussions sustained by children and adolescents is necessary to minimize the individual, societal, and economic burden of youth concussions.

The vulnerability of the brain during critical maturation periods in childhood and adolescence raises the concern that early exposure to concussion may be particularly harmful for neurodevelopment and lead to negative long-term clinical and cognitive outcomes [4]. However, the specific relationships between youth age, concussions, and their sequela are complex. Some studies show that younger age at injury (e.g., early and middle childhood) is associated with worse cognitive [5] and psychosocial [6] outcomes in later childhood years (e.g., late childhood and adolescence), as well as longer time to discharge from concussion care [7]. Contrarily, other studies find that older age at injury (e.g., late childhood and adolescence) is associated with greater post-concussive symptoms 1 month post injury [8, 9]. Further complicating the picture, additional work shows no relationship between age of first concussion (AFC) during youth and time until asymptomatic [10] or psychological and cognitive outcomes in the later childhood years [11]. It is noteworthy that the majority of these studies focus on short-term outcomes, and therefore longer-term consequences of age at concussion remain largely unknown. Specifically, the relationship between age at concussion and outcomes in young adulthood has not yet been characterized. Moreover, it is valuable to examine the relationship between age at concussion and future outcomes separately among men and women, as neurodevelopmental trajectories differ between boys and girls [12, 13], which may influence post-concussive outcomes in young adulthood. As such, the purpose of the present study was to investigate the relationship between AFC and cognitive, psychological, and physical outcomes in healthy collegiate women and men athletes using data from the National Collegiate Athletic Association (NCAA) – USA Department of Defense (DoD) Grand Alliance: Concussion Assessment, Research and Education (CARE) Consortium. The CARE Consortium provides an invaluable opportunity to investigate this research question, as it implements comprehensive methodological techniques while simultaneously recruiting and thoroughly characterizing a sample of collegiate athletes that is appreciably larger than most individual studies examining concussion-related research topics, including the role of age at injury. We hypothesized that earlier AFC would be associated with worse neurocognitive performance and postural instability, and greater psychological distress and symptoms commonly associated with concussion among both women and men.

2. Materials and Methods

2.1. Participants

Participants were recruited as part of the CARE Consortium, a 30-site, multiyear study examining the natural history of concussions in NCAA athletes and USA Service Academy cadets. Details about the CARE Consortium are described elsewhere [14].

For the present analysis, we included NCAA athletes from various contact (e.g., soccer, football, basketball, etc.), limited-contact (e.g., baseball, fencing, volleyball, etc.), and non-contact sports (e.g., swimming, tennis, golf, etc.) [15], including those at the USA service academies, from the first phase of the CARE Consortium (2014–2017) who had a baseline concussion assessment. We restricted our analyses to the first baseline assessment completed after participant enrollment. Approximately 50% of the first baseline assessments were completed on freshmen and 50% were completed on upperclassmen. Participants were excluded if they reported no prior concussions, a concussion in the last 6 months, history of moderate/severe traumatic brain injury (TBI), history of stroke, history of brain surgery, inaccurate information regarding AFC (described below), or were missing any covariates (described below). The final sample included 4,267 participants (Fig. 1). Demographics and descriptive statistics for men and women are shown in Table 1. The local IRB at each performance site, as well as the USA Army Medical Research and Materiel Command Human Research Protection Office, reviewed and approved all study procedures. All participants provided written informed consent and this study was performed in accordance with the Declaration of Helsinki.

Fig. 1.

Fig. 1

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Flow chart detailing participant inclusion/exclusion and generation of the final sample. CARE Concussion Assessment, Research and Education, NCAA National Collegiate Athletic Association, TBI traumatic brain injury

Table 1.

Demographic and descriptive statistics for men and women collegiate athletes

Women Men
(N = 1818) (N = 2449)
Age, mean (SD) 19.1 (1.27) 19.3 (1.44)
Number of previous concussions, n (%)
  1 1367 (75.2%) 1910 (78.0%)
  2 327 (18.0%) 399 (16.3%)
  3 + 124 (6.8%) 140 (5.7%)
Race/Ethnicity, n (%)
  Black 135 (7.4%) 330 (13.5%)
  Other 275 (15.1%) 374 (15.3%)
  White/Non-Hispanic 1408 (77.4%) 1745 (71.3%)
Psychiatric disorders, n (%)
  No 1616 (88.9%) 2340 (95.5%)
  Yes 202 (11.1%) 109 (4.5%)
Neurodevelopmental disorders, n (%)
  No 1639 (90.2%) 2168 (88.5%)
  Yes 179 (9.8%) 281 (11.5%)
Migraine history, n (%)
  No 1588 (87.3%) 2252 (92.0%)
  Yes 230 (12.7%) 197 (8.0%)
  SES, mean (SD) 53.9 (9.06) 52.4 (9.78)
Sport type, n (%)
  Contact sport 804 (44.2%) 1726 (70.5%)
  Limited-contact sport 560 (30.8%) 559 (22.8%)
  Non-contact sport 454 (25.0%) 164 (6.7%)
  Age of first concussion, mean (SD) 15.2 (3.06) 15.0 (3.14)
  BSI-18 Somatic, mean (SD) 1.23 (2.19) 0.832 (1.89)
  BSI-18 Depression, mean (SD) 1.05 (2.23) 0.857 (1.95)
  BSI-18 Anxiety, mean (SD) 1.29 (2.32) 0.848 (1.93)
  BSI-18 Global Severity Index, mean (SD) 3.56 (5.67) 2.54 (4.95)
  BESS, mean (SD) 12.7 (5.87) 13.6 (6.47)
  ImPACT Verbal Memory, mean (SD) 88.8 (10.1) 87.8 (10.3)
  ImPACT Visual Memory, mean (SD) 77.2 (12.9) 79.9 (12.9)
  ImPACT Visual Motor Speed, mean (SD) 42.1 (6.07) 41.6 (6.53)
  ImPACT Reaction Time, mean (SD) 0.583 (0.0786) 0.591 (0.0941)
  ImPACT PCSS Symptom Severity, mean (SD) 5.52 (8.51) 3.23 (5.99)
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BESS Balance Error Scoring System, BSI-18 Brief Symptom Inventory 18, ImPACT Immediate Post-Concussion Assessment and Cognitive Testing, PCSS Post-Concussion Symptom Scale, SES socioeconomic status

2.2. Demographics and Medical History

All participants completed the Demographics and Personal and Family Medical History form, which collects information on demographics, concussion history, and personal and family medical history. Participants are asked to self-report race/ethnicity, psychiatric disorders (i.e., depression/other mood disorders, anxiety disorders, post-traumatic stress disorder, bipolar disorder, schizophrenia/other psychotic disorders, somatoform disorder, personality disorders, and other/unknown), neurodevelopmental disorders (i.e., learning disability and attention deficit hyperactivity disorder), migraine history, number of previous concussions, age at each concussion, and estimated date of each concussion. A concussion was defined to participants as: “A change in brain function following a force to the head, which may be accompanied by temporary loss of consciousness, but is identified in awake individuals with measures of neurological and cognitive dysfunction” [16]. Participants were also presented with a list of ten common concussion symptoms and a note that “a concussion can occur without being ‘knocked out’ or unconscious” and “getting your ‘bell rung’ and ‘clearing the cobwebs’ is a concussion” [16]. AFC was defined as the age the participant self-reported being when they sustained their first concussion. Participants were excluded if the self-reported AFC and self-reported date of their first concussion differed by more than 2 years (n = 142) [17]. Self-reported AFC and self-reported date of first concussion differed by zero years in 70% of participants, 1 year in 27% of participants, and 2 years in 3% of participants. Self-reported AFC included both sport- and non-sport-related concussions. Due to small sample sizes, race/ethnicity was re-coded as White/Non-Hispanic (n = 3,153), Black (n = 465), and Other (n = 649). Finally, participants self-reported the education and occupation of their mother and father. Socioeconomic status (SES) was calculated using the Hollingshead Four-Factor Index [18]. Briefly, parental education was coded on a 7-point scale and multiplied by three, then added to the parental occupation score, which was coded on a 9-point scale and multiplied by five. Maternal and paternal SES scores were calculated separately then averaged to generate a composite SES score for each participant. If a SES score was only available for one parent, that score was used as the overall SES score for the participant.

2.3. Outcome Measures

All outcome measures are thoroughly described elsewhere [19–24]. The Brief Symptom Inventory 18 (BSI-18) was used to measure psychological distress and has been shown to be both reliable (Cronbach α = 0.75–0.91) and valid in a TBI population, specifically months to years postinjury [19], as well as in healthy high school and collegiate athletes (Cronbach α = 0.66–0.83) [20]. The BSI-18 generates a composite score, hereby referred to as the global severity index (GSI), and subscores reflecting anxiety, depression, and somatic distress dimensions [21]. The Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT), which generates composite scores for verbal memory, visual memory, visual motor speed, and reaction time, measured neurocognition. The ImPACT also assesses severity of concussion symptoms through the Post-Concussion Symptom Scale (PCSS) [22]. The Balance Error Scoring System (BESS) assessed postural stability [23, 24].

2.4. Statistical Analyses

Statistical analyses were performed using R version 3.6.1 for Macintosh. We examined the effects of AFC on each outcome measure (i.e., BSI-18 GSI and dimension subscores, ImPACT composite scores, ImPACT PCSS symptom severity score, BESS total score) among women and men using hierarchical, generalized linear models. In the first model, potentially confounding factors, including number of previous concussions, race/ethnicity, psychiatric disorder history, neurodevelopmental disorder history, migraine history, SES, and sport type, were entered as predictors. Relevant covariates to be included in model one were selected consistent with prior research [23, 25–27]. In the second model, AFC was added to the existing model. All models were run separately for men and women, given the different neurodevelopmental trajectories between boys and girls [12, 13]. Reported results refer to the output of the second model, as we were primarily interested in the effects of each predictor after adjusting for all other predictors (Tables 2 and 3). Models were fit based on the error distribution of the response variables. The best fitting model (i.e., lowest Akaike information criterion value [23]) is reported in the results. For both men and women, a Gaussian distribution best fit the ImPACT verbal memory, visual memory, and visual motor speed composite scores. For both men and women, a negative binomial distribution best fit the BSI-18 GSI, anxiety, depression, and somatic subscores, BESS score, and ImPACT PCSS symptom severity score. For both men and women, an inverse Gaussian distribution best fit the ImPACT reaction time composite score. Uncorrected significance was defined as P < 0.05. To account for multiple comparisons across the outcome measures, we performed a Bonferroni correction for ten comparisons; corrected significance was defined as P < 0.005. To assess for outliers, we also replicated analyses after excluding individuals with studentized residuals > 3 or < − 3. Results were comparable and therefore the reported results do not exclude outliers.

Table 2.

Results of the hierarchical, generalized linear models for outcomes from women

Predictor BESS
 BSI-18 Global Severity Index
 BSI-18 Anxiety
 BSI-18 Depression
 BSI-18 Somatic
Exp(B) 95% CI Exp(B) 95% CI Exp(B) 95% CI Exp(B) 95% CI Exp(B) 95% CI
2 previous concussions 1.03 0.97 – 1.09 1.11 0.92 – 1.35 1.22 0.99 – 1.52 0.97 0.75 – 1.27 1.13 0.91 – 1.42
3 + previous concussions 0.94 0.85 – 1.03 1.35* 1.02 – 1.81 1.40* 1.02 – 1.94 1.36 0.94 – 2.02 1.28 0.92 – 1.81
Black Race/Ethnicity 1.07 0.99 – 1.17 1.02 0.78 – 1.37 0.76 0.55 – 1.06 1.08 0.75 – 1.59 1.28 0.94 – 1.79
Other Race/Ethnicity 0.99 0.93 – 1.05 1.12 0.92 – 1.38 1.01 0.80 – 1.27 1.11 0.85 – 1.46 1.27* 1.01 – 1.62
Psychiatric disorder 1.03 0.96 – 1.11 2.07** 1.66 – 2.61 2.34** 1.83 – 3.00 2.70** 2.04 – 3.64 1.36* 1.05 – 1.78
Neurodevelopmental disorder 1.01 0.94 – 1.09 1.44** 1.14 – 1.84 1.47** 1.13 – 1.93 1.35 0.99 – 1.88 1.48* 1.13 – 1.96
Migraine 0.99 0.93 – 1.06 1.34* 1.09 – 1.67 1.26 0.99 – 1.61 1.26 0.95 – 1.69 1.52** 1.20 – 1.96
SES 1 1.00 – 1.00 1 0.99 – 1.00 1 0.99 – 1.01 1 0.99 – 1.01 0.99 0.98 – 1.00
Limited-contact sport 0.99 0.93 – 1.05 0.91 0.75 – 1.11 1 0.80 – 1.25 0.93 0.72 – 1.20 0.83 0.66 – 1.04
Contact sport 1.03 0.97 – 1.09 0.73** 0.61 – 0.87 0.88 0.71 – 1.07 0.63** 0.49 – 0.81 0.67** 0.55 – 0.83
AFC 1 0.99 – 1.01 0.96** 0.94 – 0.98 0.96* 0.94 – 0.99 0.97* 0.93 – 1.00 0.96** 0.93 – 0.99
Observations 1705 1807 1807 1807 1807
Overall model LRT = 13.66 LRT = 112.75** LRT = 93.58** LRT = 95.38** LRT = 70.82**
Distribution Negative binomial Negative binomial Negative binomial Negative binomial Negative binomial
Predictor ImPACT PCSS
 ImPACT Verbal Memory
 ImPACT Visual Memory
 ImPACT Visual Motor Speed
 ImPACT Reaction Time
Exp(B) 95% CI B 95% CI B 95% CI B 95% CI B 95% CI
2 previous concussions 1.15 0.93 – 1.45 1.71* 0.34 – 3.08 0.86 − 0.89 – 2.61 0.72 − 0.10 – 1.53 − 0.0126* − 0.0245 – −0.0003
3 + previous concussions 1.11 0.80 – 1.58 2.10* 0.01 – 4.20 3.60* 0.94 – 6.27 1.62* 0.38 – 2.87 − 0.0303** − 0.0473 – −0.0123
Black Race/Ethnicity 1.05 0.77 – 1.47 − 1.85 − 3.85 – 0.16 − 1.27 − 3.82 – 1.29 − 1.04 − 2.23 – 0.15 0.0285** 0.0097 – 0.0486
Other Race/Ethnicity 1.24 0.99 – 1.57 0.69 − 0.72 – 2.10 0.26 − 1.54 – 2.06 − 0.1 − 0.94 – 0.73 0.0081 − 0.0046 – 0.0212
Psychiatric disorder 1.42* 1.10 – 1.86 − 0.90 − 2.56 – 0.76 − 0.24 − 2.35 – 1.87 − 0.05 − 1.03 – 0.93 − 0.0035 − 0.0178 – 0.0114
Neurodevelopmental disorder 1.63** 1.23 – 2.21 − 1 − 2.85 – 0.84 − 1.55 − 3.89 – 0.80 − 2.34** − 3.44 – − 1.25 0.0187* 0.0018 – 0.0365
Migraine 1.38* 1.08 – 1.79 0.62 − 0.96 – 2.20 − 0.46 − 2.47 – 1.56 0.26 − 0.68 – 1.20 − 0.0036 − 0.0172 – 0.0108
SES 1 0.99 – 1.01 0.07* 0.01 – 0.13 0.07 − 0.01 – 0.14 0.07** 0.03 – 0.10 − 0.0003 − 0.0008 – 0.0003
Limited-contact sport 0.65** 0.52 – 0.81 0.92 − 0.50 – 2.34 0.96 − 0.85 – 2.77 0.34 − 0.50 – 1.19 − 0.0063 − 0.0191 – 0.0065
Contact sport 0.62** 0.50 – 0.76 1.62* 0.31 – 2.93 3.34** 1.67 – 5.00 1.03* 0.25 – 1.81 − 0.0042 − 0.0161 – 0.0075
AFC 0.97* 0.94 – 1.00 0.03 − 0.15 – 0.20 − 0.03 − 0.25 – 0.19 0.06 − 0.04 – 0.17 − 0.0027** − 0.0043 – −0.0011
Observations 1445 1467 1467 1467 1466
Overall model LRT = 64.60** F = 2.76** F = 3.14** F = 4.97** F = 3.24**
Distribution Negative binonrial Gaussian Gaussian Gaussian Inverse Gaussiain
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AFC age of first concussion, BESS Balance Error Scoring System, BSI-18 Brief Symptom Inventory 18, ImPACT Immediate Post-Concussion Assessment and Cognitive Testing, LRT Likelihood ratio test, PCSS Post-Concussion Symptom Scale, SES socioeconomic status

*

P < 0.05,

**

P < 0.005

Table 3.

Results of the hierarchical, generalized linear models for outcomes from men

Predictor BESS
 BSI-18 Global Severity Index
 BSI-18 Anxiety
 BSI-18 Depression
 BSI-18 Somatic
Exp(B) 95% CI Exp(B) 95% CI Exp(B) 95% CI Exp(B) 95% CI Exp(B) 95% CI
2 previous concussions 1.03 0.97 – 1.08 1.15 0.93 – 1.42 1.18 0.93 – 1.52 1.10 0.86 – 1.43 1.15 0.90 – 1.48
3 + previous concussions 1.02 0.93 – 1.11 0.96 0.69 – 1.36 0.92 0.63 – 1.39 0.96 0.65 – 1.47 1.01 0.68 – 1.53
Black Race/Ethnicity 1.02 0.97 – 1.09 1.08 0.86 – 1.37 0.90 0.68 – 1.19 1.33* 1.01 – 1.77 1.03 0.78 – 1.36
Other Race/Ethnicity 0.98 0.93 – 1.04 0.97 0.79 – 1.22 1.06 0.83 – 1.37 1.09 0.85 – 1.43 0.78 0.60 – 1.02
Psychiatric disorder 0.99 0.90 – 1.09 2.40** 1.67 – 3.55 2.57** 1.72 – 3.98 2.69** 1.79 – 4.21 1.95** 1.27 – 3.09
Neurodevelopmental disorder 1.06 0.99 – 1.12 0.99 0.77 – 1.27 1.01 0.77 – 1.36 1 0.75 – 1.34 0.96 0.72 – 1.30
Migraine 0.95 0.89 – 1.02 1.35* 1.03 – 1.82 1.22 0.88 – 1.70 1.29 0.93 – 1.83 1.59* 1.15 – 2.23
SES 1 1.00 – 1.00 1.01 1.00 – 1.02 1.01* 1.00 – 1.02 1.00 1.00 – 1.01 1.01 1.00 – 1.02
Limited-contact sport 1 0.92 – 1.09 0.91 0.65 – 1.27 1.06 0.71 – 1.55 0.83 0.56 – 1.22 0.87 0.58 – 1.29
Contact sport 0.98 0.91 – 1.07 0.79 0.57 – 1.06 0.90 0.62 – 1.28 0.67* 0.46 – 0.95 0.82 0.56 – 1.17
AFC 1 1.00 – 1.01 1 0.97 – 1.02 0.98 0.95 – 1.01 1.01 0.98 – 1.04 1 0.97 – 1.03
Observations 2312 2427 2427 2427 2427
Overall model LRT = 9.67 LRT = 52.99** LRT = 50.16** LRT = 47.49** LRT = 34.74**
Distribution Negative Binomial Negative Binomial Negative Binomial Negative Binomial Negative Binomial
Predictor ImPACT PCSS
 ImPACT Verbal Memory
 ImPACT Visual Memory
 ImPACT Visual Motor Speed Time
 ImPACT Reaction
Exp(B) 95% CI B 95% CI B 95% CI B 95% CI B 95% CI
2 previous concussions 1.09 0.85 – 1.42 1.31* 0.04 – 2.59 − 0.02 − 1.62 – 1.58 1.15* 0.35 – 1.95 − 0.0083 − 0.0214 – 0.0053
3 + previous concussions 1.29 0.88 – 1.97 1.10 − 0.93 – 3.13 1.87 − 0.69 – 4.43 1.07 − 0.20 – 2.35 − 0.0068 − 0.0273 – 0.0151
Black Race/Ethnicity 0.91 0.70 – 1.20 − 3.55** − 4.96 – − 2.14 − 4.83** − 6.60 – − 3.06 − 2.87** − 3.76 – − 1.99 0.0503** 0.0336 – 0.0676
Other Race/Ethnicity 1.26 0.99 – 1.63 − 0.48 − 1.74 – 0.78 − 1.24 − 2.82 – 0.35 − 0.17 − 0.96 – 0.63 0.0157* 0.0022 – 0.0298
Psychiatric disorder 2.13** 1.40 – 3.39 0.75 − 1.57 – 3.06 − 1.36 − 4.26 – 1.54 0.65 − 0.80 – 2.10 − 0.0136 − 0.0360 – 0.0111
Neurodevelopmental disorder 1.22 0.93 – 1.64 − 3.55** − 5.01 – − 2.09 − 3.50** − 5.33 – − 1.66 − 2.24** − 3.16 – − 1.32 0.0232* 0.0072 – 0.0400
Migraine 1.64** 1.19 – 2.31 − 0.52 − 2.21 – 1.17 − 0.03 − 2.15 – 2.09 − 0.09 − 1.15 – 0.97 − 0.0089 − 0.0258 – 0.0090
SES 1 0.99 – 1.01 − 0.02 − 0.07 – 0.02 0.02 − 0.04 – 0.08 0.06** 0.03 – 0.09 − 0.0008** − 0.0013 – − 0.0003
Limited-contact sport 0.65* 0.43 – 0.95 1.39 − 0.67 – 3.46 1.60 − 0.99 – 4.19 0.54 − 0.76 – 1.83 − 0.0114 − 0.0340 – 0.0100
Contact sport 0.57** 0.39 – 0.82 1.76 − 0.17 – 3.70 2.48* 0.05 – 4.91 0.97 − 0.25 – 2.18 − 0.0064 − 0.0279 – 0.0136
AFC 0.98 0.95 – 1.01 0.15 − 0.01 – 0.30 − 0.05 − 0.25 – 0.14 0.02 − 0.08 – 0.11 − 0.0005 − 0.0022 – 0.0012
Observations 1870 1911 1909 1911 1910
Overall model LRT = 54.64** F = 4.84** F = 4.74** F = 9.26** F = 6.58**
Distribution Negative Binomial Gaussian Gaussian Gaussian Inverse Gaussiim
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AFC age of first concussion, BESS Balance Error Scoring System, BSI-18 Brief Symptom Inventory 18, ImPACT Immediate Post-Concussion Assessment and Cognitive Testing, LRT Likelihood ratio test, PCSS Post-Concussion Symptom Scale, SES socioeconomic status

*

P < 0.05,

**

P < 0.005

Parameter estimates generated and reported vary based on the data distribution [23]. A generalized linear model best fit with a Gaussian (i.e., normal) distribution is equivalent to a linear regression model and therefore the reported parameter estimates are B coefficients. Similarly, the reported parameter estimates of a generalized linear model best fit with an inverse Gaussian distribution are also B coefficients. A positive B coefficient suggests a higher and a negative B coefficient suggests a lower score on the outcome variable for a given predictor variable. For example, among women, the ImPACT reaction time B = − 0.003 for AFC (Table 2), which suggests that after adjusting for all other predictors in the model, every 1-year increase in AFC (i.e., sustained first injury at an older age) is associated with a decrease in ImPACT reaction time by 0.003 s (reflecting faster reaction time). For generalized linear models best fit with a negative binomial distribution, the reported parameter estimates are Exp(B), which is interpreted as the percentage the outcome variable increases or decreases with a given predictor variable. For example, among women, the BSI-18 somatic subscore Exp(B) = 0.96, which suggests that after adjusting for all other predictors in the model, every 1-year increase in AFC is associated with a 4% decrease in BSI-18 somatic subscore.

3. Results

3.1. Women: Age of First Concussion (AFC)

Among women, the average time from AFC to the baseline assessment was 3.88 years. The average AFC was 15.19 years (range = 1–22 years) and the average age at the baseline assessment was 19.07 (range = 17 25 years). Later AFC, which reflects older age at first injury, was associated with lower (better) BSI-18 GSI (Exp(B) = 0.96, P = 0.001; Fig. 2a) and somatic (Exp(B) = 0.96, P = 0.002; Fig. 2b) subscores, as well as faster (better) ImPACT reaction time (B = − 0.003, P = 0.001; Fig. 2c), which all survived multiple comparisons (Table 2). Later AFC was also associated with lower (better) BSI-18 depression (Exp(B) = 0.97, P = 0.037) and anxiety (Exp(B) = 0.96, P = 0.006) subscores, along with lower (better) ImPACT PCSS symptom severity scores (Exp(B) = 0.97, P = 0.035), which did not survive multiple comparisons (Table 2).

Fig. 2.

Fig. 2

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Scatterplots depicting relationship between AFC (x-axis) and a women’s BSI-18 GSI, b women’s BSI-18 somatic, c women’s ImPACT reaction time. AFC age of first concussion, BSI-18 Brief Symptom Inventory 18, GSI global severity index, ImPACT Immediate Post-Concussion Assessment and Cognitive Testing

3.2. Women—Other Contributing Factors

Many of the potentially confounding factors included in the analyses were associated with baseline concussion assessments (Table 2); for brevity, only those that survived multiple comparisons are reported below. Compared to having one previous concussion, having three + previous concussions was associated with faster (better) ImPACT reaction time (B = − 0.03, P < 0.001). Compared to White/Non-Hispanic race/ethnicity, Black race was associated with slower (worse) ImPACT reaction time (B = 0.03, P = 0.004). Positive psychiatric disorder history was associated with higher (worse) BSI-18 GSI (Exp(B) = 2.07, P < 0.001), anxiety (Exp(B) = 2.34, P < 0.001), and depression (Exp(B) = 2.70, P < 0.001) subscores. Positive neurodevelopmental disorder history was associated with worse BSI-18 GSI (Exp(B) = 1.44, P = 0.003) and anxiety (Exp(B) = 1.47, P = 0.004) subscores, as well as worse ImPACT visual motor speed (B = − 2.34, P < 0.001) and PCSS symptom severity (Exp(B) = 1.63, P < 0.001) scores. Positive migraine history was associated with higher (worse) BSI-18 somatic subscores (Exp(B) = 1.52, P < 0.001). Higher SES was associated with higher (better) ImPACT visual motor speed (B = 0.07, P < 0.001). Compared to non-contact sports, limited-contact sports were associated with lower (better) ImPACT PCSS symptom severity (Exp(B) = 0.65, P < 0.001) and contact sports were associated with lower (better) BSI-18 GSI (Exp(B) = 0.73, P < 0.001), somatic (Exp(B) = 0.67, P < 0.001), and depression (Exp(B) = 0.63, P < 0.001) subscores, along with better ImPACT PCSS symptom severity (Exp(B) = 0.62, P < 0.001) and visual memory (B = 3.34, P < 0.001) scores.

3.3. Men—AFC

Among men, the average time from AFC to the baseline assessment was 4.36 years. The average AFC was 14.95 years (range = 1–25 years) and the average age at the baseline assessment was 19.31 (range = 17–28 years). AFC was not associated with any clinical outcomes (Table 3).

3.4. Men—Other Contributing Factors

Many of the potentially confounding factors included in the analyses were associated with baseline concussion assessments (Table 3); for brevity, only those that survived multiple comparisons are reported below. Compared to White/Non-Hispanic race/ethnicity, Black race was associated with worse ImPACT verbal memory (B = − 3.55, P < 0.001), visual memory (B = − 4.83, P < 0.001), visual motor speed (B = − 2.87, P < 0.001), and reaction time (B = 0.05, P < 0.001) composite scores. Positive psychiatric disorder history was associated with higher (worse) BSI-18 GSI (Exp(B) = 2.40, P < 0.001), anxiety (Exp(B) = 2.57, P < 0.001), depression (Exp(B) = 2.69, P < 0.001), and somatic (Exp(B) = 1.95, P = 0.002) subscores, as well as higher (worse) ImPACT PCSS symptom severity scores (Exp(B) = 2.13, P < 0.001). Positive neurodevelopmental disorder history was associated with lower (worse) ImPACT verbal memory (B = −3.55, P < 0.001), visual memory (B = − 3.50, P < 0.001), and visual motor speed (B = − 2.24, P < 0.001) composite scores. Positive migraine history was associated with higher (worse) ImPACT PCSS symptom severity scores (Exp(B) = 1.64, P = 0.003). Higher SES was associated with higher (better) ImPACT visual motor speed (B = 0.06, P < 0.001) and faster (better) reaction time (B = − 0.0008, P = 0.004) composite scores. Compared to non-contact sports, contact sports were associated with lower (better) ImPACT PCSS symptom severity scores (Exp(B) = 0.57, P = 0.003).

4. Discussion

This study examined the relationship between AFC and ten diverse cognitive, physical, and psychological outcomes in healthy collegiate men and women athletes recruited as part of the CARE Consortium. Among women, later AFC was associated with faster reaction time as well as lower global and somatic psychological distress, after adjusting for concussion history, sport type, pre-existing conditions, and sociodemographic factors. Among men, there were no significant relationships between AFC and clinical/cognitive outcomes after adjusting for concussion history, sport type, pre-existing conditions, and sociodemographic factors. Although these results among women were statistically significant, they are likely not clinically meaningful. Sport type, pre-existing conditions, and sociodemographic disparities may impact clinical and cognitive outcomes in collegiate athletes more than concussion history.

While the relationships between AFC and some clinical outcomes were statistically significant in women even after adjusting for relevant covariates and applying the strict Bonferroni correction, these findings are unlikely to be clinically relevant, as evidenced by the small model coefficients. Specifically, among women, every 1-year increase in AFC was associated with a 4% decrease in BSI-18 somatic (mean score = 1.23) and global (mean score = 3.56) subscores. The BSI-18 somatic and global subscores are scored from 0 to 24 and 0 to 72, respectively. Therefore, a 4% change in psychological distress is associated with less than a 1-point change on the BSI-18 somatic subscore and less than a 3-point change on the BSI-18 global score. Moreover, among women, every 1-year increase in AFC was associated with a decrease in reaction time by 0.003 s. Youth sports have numerous benefits (e.g., physical health, psychosocial development, and motor skill development [28]); however, there are concerns about the safety of youth sports due to the risk of head injury and corresponding sequela [29, 30]. The findings in this study suggest that these athletes may not experience lasting clinical deficits due to earlier AFC or AFC may have minimal clinical relevance after accounting for numerous other factors associated with clinical outcomes (i.e., concussion history, sociodemographic factors, pre-existing conditions, and sport type) in current collegiate athletes.

Previous work demonstrates complex relationships between age at concussion and negative outcomes. Some studies show that younger age at injury (i.e., early and middle childhood) is associated with poorer post-injury outcomes in the weeks and months following the initial injury [5, 7], as well as throughout childhood and adolescence [5, 6], while other studies show that older age at injury (i.e., late childhood and adolescence) is associated with poorer outcomes 1 month following the initial injury [8, 9]. Additional work demonstrates no relationship between age at injury in youth years (i.e., early childhood through adolescence) and recovery throughout the first month post-injury [10, 31] or cognitive outcomes in the years following the injury [11]. The present study addresses a critical gap in the literature by examining clinical outcomes in young adulthood, as opposed to strictly during childhood and adolescence. Findings demonstrated no clinically meaningful associations between AFC and clinical outcome measures after adjusting for relevant background variables (i.e., concussion history, sport type, pre-existing conditions, and sociodemographic factors). Nonetheless, it is important to minimize the risk of concussions in youth sports to optimize brain development and future clinical outcomes, which may include implementing rule changes, improving equipment, and eliminating unnecessary contact [32]. Moreover, increasing medical coverage at youth sporting events may reduce delayed reporting and/or undiagnosed concussions, and consequently improve recovery and outcomes following concussions [33, 34].

Although AFC is not associated with clinically relevant consequences in young adulthood, clinical deficits may manifest with age; concussions may be associated with adverse consequences later in life, including increased risk for neurodegenerative diseases [35], psychiatric symptoms [36], neurobehavioral symptoms, and cognitive decline [37]. Moreover, previous work has identified a relationship between AFC during youth and psychiatric morbidity, social outcomes, educational attainment, and premature morbidity during adulthood [38]. As such, it is imperative to examine the relationship between AFC and cognitive, psychological, and physical outcomes with age, either by following this cohort throughout adulthood or by replicating these analyses in an independent cohort of middle- and late-life adults. Furthermore, because there is conflicting evidence regarding sex differences in post-concussive outcomes [39–41] and because neuroimaging studies routinely demonstrate that girls exhibit a slower rate of neurodevelopmental changes than boys, including slower gray matter pruning, white matter increases, and cerebral blood flow decreases [12, 13], it is critical that future work continues to examine sex as a biological variable in determining the relationship between AFC and later-in-life outcomes.

This study also examined the relationship between clinical outcomes and concussion history, sociodemographic factors, pre-existing conditions, and sport type, demonstrating that most of these factors contribute substantially to clinical outcomes in young adulthood. Surprisingly, greater concussion history was associated with faster reaction time in women. This may be due to practice effects, as these athletes may have taken the ImPACT more times than athletes reporting only one previous concussion. Alternatively, individuals with faster reaction times may opt to participate in sports typically associated with increased risk for concussion, such as soccer, over sports with lower risk for concussion, such as swimming [42], although additional work is needed to investigate this hypothesis. Moreover, number of previous concussions was not associated with any negative consequences. Some evidence suggests concussion history is associated with lower neuropsychological performance in college football players [43], whereas other evidence, more consistent with results reported here, suggests concussion history does not have neurocognitive consequences in current collegiate athletes [25].

Sociodemographic factors were associated with neurocognitive performance; Black race/ethnicity and lower SES were independently associated with lower neurocognitive scores in men and women, similar to previous findings [25], further underscoring the importance of considering sociodemographic factors to better understand neurocognition in collegiate athletes. The observed relationships between these social determinants of health and neurocognition are best explained by the systemic disparities and racial inequities within the USA and its healthcare system [44].

Pre-existing conditions influenced clinical symptoms and cognitive performance. Positive psychiatric history and migraine history were independently associated with greater clinical symptoms in women and men, which is consistent with research demonstrating these factors influence concussion-like symptoms in healthy high school [45] and collegiate [46] athletes. Positive neurodevelopmental disorder history was also associated with greater clinical symptoms in women, and lower neurocognitive scores in women and men. Previous studies demonstrate that neurodevelopmental disorder history contributes to concussion-related symptoms and neurocognitive performance at baseline [25, 45, 47]. Our findings further demonstrate that pre-existing conditions are important to consider when examining individual variability in cognitive and clinical symptoms during young adulthood.

Finally, compared to non-contact sports, contact sports were associated with fewer clinical symptoms in women and men, along with better neurocognitive performance in women, which is consistent with previous findings [23]. Similarly, limited-contact sports were associated with fewer concussion-related symptoms in women. There may be clinical and cognitive benefits of participating in team sports [48, 49], which are typically contact or limited-contact sports, while non-contact sports are typically individual in nature. Together, these findings suggest that sport type, pre-existing conditions, and sociodemographic disparities may impact clinical and cognitive outcomes more than concussion history and underscore the importance of considering these factors in clinical and research settings to better understand concussion symptomology and neurocognition.

This study has some limitations. First, we relied on self-report for many parameters, which is inherently prone to bias. This is particularly a limitation for self-reported concussion history, specifically during childhood where there is often inadequate medical coverage at youth sporting events, which may increase the prevalence of undiagnosed and unreported concussions. However, self-report is common in behavioral/medical research and is a limitation in many studies [50]. Second, it is unknown how results generalize to individuals who did not meet inclusion criteria, such as populations other than NCAA student athletes (i.e., younger and older cohorts)—particularly in the context of aging. The majority of injuries occurred during adolescence and pre-adolescence and therefore it is unclear how these results generalize to injuries sustained earlier in life, such as those sustained in early childhood. Future research should investigate the relationship between sustaining a concussion during certain critical neurodevelopmental periods (e.g., early childhood) and clinical outcomes in young adulthood, as some work suggests that neurodevelopmental stages, as opposed to strictly age, are related to shorter-term, post-concussive outcomes [51–54]. Third, sports participation throughout youth and at AFC may be relevant considerations in this study; however, sport played at AFC was not collected as part of the CARE Consortium and there are many combinations of sports participation at youth ages that could not pragmatically be adjusted for in the present analyses. Fourth, these findings do not consider differences in clinical outcomes between individuals with and without a positive concussion history, which is outside the scope of this study, but should be investigated in future work. Finally, the clinical measures in this study assess acute concussion symptomology and may not adequately capture more chronic patient-reported outcomes.

5. Conclusion

We report that after considering the effects of concussion history, sport type, pre-existing conditions, and sociodemographic disparities, later AFC is associated with lower global and somatic psychological distress and faster reaction time in women that is statistically significant but likely not clinically meaningful. AFC is not related to other clinical outcomes in women or men, including severity of concussion-related symptoms, postural stability, anxious psychological distress, depressive psychological distress, visual memory, verbal memory, and visual motor speed. Additional research should investigate the effects of AFC later in life, such as in middle and older adulthood. This study also showed that pre-existing conditions, sociodemographic factors, and sport type have a greater impact on clinical outcomes than concussion history.

Key Points.

Older age of first concussion was associated with less psychological distress and faster reaction time in collegiate women.

Age of first concussion was not associated with cognitive, psychological, or physical outcomes in collegiate men.

The small coefficients suggest that while age of first concussion is associated with statistically significant differences in clinical outcomes among collegiate women, these results are likely not clinically meaningful; sport type, pre-existing conditions, and sociodemographic disparities may impact clinical and cognitive outcomes in young adulthood more than concussion history.

Contributing CARE Consortium Investigators Include:

April Marie (Reed) Hoy, MS, ATC (Azusa Pacific University); Darren Campbell, MD (Brigham Young University); Louise A. Kelly, PhD (California Lutheran University); John DiFiori, MD (Hospital for Special Surgery, National Basketball Association); Justus D. Ortega, PhD (Humboldt State University); Nicholas Port, PhD (Indiana University); Margot Putukian MD (Major League Soccer); T. Dianne Langford, PhD and Jane McDevitt, PhD, ATC, CSCS (Temple University); Christopher C. Giza, MD (University of California, Los Angeles); Holly J. Benjamin MD (University of Chicago); Thomas W. Kaminski, PhD, ATC (University of Delaware); James R. Clugston, MD, MS (University of Florida); Joseph B. Hazzard, Jr., ATC (University of Houston-Clear Lake); Patrick G. O’Donnell, MHA (University of Massachusetts Memorial Medical Center); Luis A Feigenbaum, PT, DPT, ATC (University of Miami); James T. Eckner, MD, MS (University of Michigan); Jason P. Mihalik, PhD, CAT(C), ATC (University of North Carolina at Chapel Hill); Christina L. Master, MD (University of Pennsylvania); Anthony P. Kontos, PhD and Michael Collins, PhD (University of Pittsburgh Medical Center); Sara P.O. Chrisman, MD, MPH (University of Washington); Alison Brooks, MD, MPH (University of Wisconsin-Madison); Jonathan Jackson, MD and Gerald McGinty, PT, DPT (United States Air Force Academy); Carlos Estevez, DPT, OCS, ECS (United States Coast Guard Academy); Kenneth L. Cameron, PhD, MPH, ATC (United States Military Academy); Adam Susmarski, DO (United States Naval Academy); Christopher M. Miles, MD (Wake Forest University); Laura Lintner DO (Winston-Salem University).

Funding

Data collection and sharing for this project was conducted with support from the National Collegiate Athletic Association (NCAA) and the Department of Defense (DOD). The US Army Medical Research Acquisition Activity, 820 Chandler Street, Fort Detrick MD 21702–5014 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 Combat Casualty Care Research Program, endorsed by the Department of Defense, through the Joint Program Committee 6/ Combat Casualty Care Research Program – Psychological Health and Traumatic Brain Injury Program under Award No. W81XWH1420151. Opinions, interpretations, conclusions and recommendations are those of the author and are not necessarily endorsed by the Department of Defense. This work was supported by the National Institute on Aging (NIA) of the National Institutes of Health (NIH) R01AG058822 (to JPH), and The Ohio State University Discovery Themes Chronic Brain Injury Initiative (JPH and JBC). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

Footnotes

Conflict of interest All of the authors declare that they have no conflicts of interest to disclose.

Ethics approval The local IRB at each performance site, as well as the US Army Medical Research and Materiel Command Human Research Protection Office, reviewed and approved all study procedures. This study was performed in accordance with the Declaration of Helsinki.

Consent to participate All participants provided written informed consent prior to participation in this study.

Availability of data

The CARE Consortium dataset used in the present study is available in the FITBIR repository (https://fitbir.nih.gov/).

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The CARE Consortium dataset used in the present study is available in the FITBIR repository (https://fitbir.nih.gov/).

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