Exposure to Head Impacts and Cognitive and Behavioral Outcomes in Youth Tackle Football Players Across 4 Seasons

Key Points Question Are repetitive head impacts in youth tackle football across 4 years of play associated with cognitive and behavioral difficulties? Findings In this cohort study including 70 male participants aged 9 to 12 years, few associations were found between cumulative head impacts and cognitive and behavioral outcomes, and no associations were seen consistently or became more prominent over the years. Meaning Because head impacts were not associated with measured outcomes, these findings suggest that other factors, including premorbid medical conditions, should be further explored.


Introduction
Repetitive subconcussive head impacts during childhood have been implicated in the development of chronic cognitive and behavioral problems. However, both retrospective 1-7 and prospective [8][9][10][11][12] research studies have yielded conflicting results regarding the association between repetitive head impacts and cognitive and behavioral outcomes.

Key Points
Question Are repetitive head impacts in youth tackle football across 4 years of play associated with cognitive and behavioral difficulties?
Findings In this cohort study including 70 male participants aged 9 to 12 years, few associations were found between cumulative head impacts and cognitive and behavioral outcomes, and no associations were seen consistently or became more prominent over the years.
Meaning Because head impacts were not associated with measured outcomes, these findings suggest that other factors, including premorbid medical conditions, should be further explored.
Previous studies [8][9][10]13 in pre-high school athletes have generally examined 1 year of head impact exposure. We conducted a 4-year prospective study in youth tackle football players. We previously reported few associations between measured head impacts and neurobehavioral outcomes over the course of 3 seasons of play. 11 The current study sought to identify associations between cognitive and behavioral outcomes and head impacts measured in youth tackle football players over 4 seasons of play.

Participants
This cohort study was approved by the IntegReview institutional review board. Written consent and assent were obtained from a parent and all participants, respectively. This study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guideline.
A local youth tackle football program was identified through community engagement; the program leadership and coaches expressed interest in participating in research examining the safety of youth tackle football. The fifth and sixth grade teams were selected for this study at the recommendation of the coaches to prioritize young age but also large team size. Players entering the fifth and sixth grades were enrolled in the summer of 2016 and followed through the fall football

Impact Monitoring
Head impacts were monitored using helmet-based Riddell InSite sensors during practices and games.
InSite sensors were first developed to quantify blunt force trauma and overpressurization from military blast injuries. 14 They characterize linear acceleration using ferroelectret films that produce an electrical charge that is proportional to the deformation of the sensor during an impact event. The relationship between sensor deformation and head acceleration is based on direct comparison testing showing a strong correlation between InSite sensors and accelerometers embedded in Hybrid III head forms (r 2 , 0.900-0.963). 15 In the current study, a head impact was defined as any impact detected by the InSite sensor. During season 1, the sensors detected impacts greater than or equal to 10 gravitational force equivalents (g). As a result of a change in the manufacturer's software to account for changes in the manufacturing process of the ferroelectret film, during seasons 2 to 4 the sensors detected impacts greater than or equal to 15g. The cumulative impact for each player for each season was calculated according to previously reported methods. 11,12 Neurocognitive and Behavioral Assessments Before and after each football season, players completed several cognitive and behavioral assessments ( Table 1). The Medical Symptom Validity Test was used at each visit to screen for response validity.
Previous medical diagnoses, including headaches, migraines, attention-deficit/hyperactivity disorder (ADHD), anxiety, depression, and number of prior concussions, were recorded at the pre-season 1 visit. Interval concussions were documented at follow-up visits. At the final post-season 4 visit, players reported whether they played other contact sports (defined as wrestling, ice hockey, soccer, lacrosse, or rugby).

Statistical Analysis
Three players were excluded from statistical analyses at the corresponding assessment time point because of Medical Symptom Validity Test failure (2 players before season 1 and 1 player after season 1). Because of missing impact data, additional players were excluded from statistical analyses involving the corresponding season's cumulative impact (9 players in season 1 and 3 players in season 4).

JAMA Network Open | Neurology
In previous reports, 9,11,12 we found several outcome measures suggesting a potential association with cumulative impact. On the basis of these results and associations found in other studies, 8,16 we narrowed the list of outcome measures in the current analysis to the 10 most likely to be affected by repetitive head impacts (Table 1).
To examine the potential for attrition bias, independent-samples 2-sided t tests and χ 2 tests

Associations Between Cumulative Impact Over Time and Outcome Scores
When assessing the association of cumulative impact measured in all previous years up to each assessment time point, few associations were significant ( Table 3). Higher cumulative impact was associated with lower Sport Concussion Assessment Tool-3 symptom scores after season 1 and before season 2, but higher scores before season 3. At the pre-season 3 time point, higher cumulative impact was also associated with worse concentration on Test of Variables of Attention.   with the between-group difference often becoming more prominent as the study progressed.
Players with a history of anxiety or depression had worse scores on the Wechsler Abbreviated Scale of Intelligence Full-Scale Intelligence Quotient-2 or Strengths and Difficulties Questionnaire Total Difficulties at 6 of 8 and 5 of 8 time points, respectively.   Discussion Some previous retrospective studies 3,4 have suggested that exposure to repetitive head impacts in tackle football before the age of 12 years is associated with neurobehavioral and cognitive problems later in life. However, other studies 1,2,6,7 have found no association between earlier age of exposure to tackle football or other contact sports and deleterious outcomes. Additionally, current high school and collegiate athletes with head impact exposure before age 12 years have not been shown to have worse neurocognitive performance than those with exposure after age 12 years. 17 Here we contribute evidence from children who were aged 9 to 12 years at enrollment that repetitive head impacts in youth tackle football were not found to be associated with neurocognitive performance or behavioral outcomes. Although outcomes on a computerized measure of processing speed (CogState) declined over the course of this study, a well-validated measure of processing speed (Wechsler Intelligence Scale for Children 5th Edition coding) improved over time, and neither change was associated with head impacts. To our knowledge, this is the longest prospective study to date to measure head impacts and neurocognitive outcomes in youth contact sport athletes.
Consistent with the first 3 years of this study, our findings from 4 seasons of play did not identify an association between cumulative head impact and neurocognitive outcomes.

Limitations
This study has limitations that should be considered. First, premorbid medical diagnoses were reported by the player and a parent, but formal diagnostic criteria were not verified. Second, the attrition of players over time limited the statistical power in the final years of the study. To reduce the effect of the decreasing sample size over time and to reduce the likelihood of type I error associated with multiple comparisons, we analyzed only the 10 outcome measures conceptually associated with repetitive head impacts. In addition, players who dropped out of the study did not differ from those who continued through all 4 years. Third, all impact sensors have limitations, and we have previously described the characteristics of the Riddell InSite sensors. 9,11, 12 We did not confirm each helmet impact with video recordings of practices and games. Fourth, although this was a prospective study spanning 4 years, we were unable to determine long-term neurocognitive outcomes in our participants. Future prospective studies could measure head impacts and monitor outcomes throughout life.

Conclusions
In conclusion, we did not find compelling evidence that cumulative head impacts across 4 years of play are associated with neurocognitive function in youth tackle football players. Rather, selfreported medical diagnoses, especially ADHD, anxiety, and depression, were consistently associated with worse neurocognitive outcomes. Over time, neurocognitive performance appears to be influenced by comorbid medical diagnoses more than by repetitive head impacts.